Skip to main content

Advertisement

SpringerLink
Log in

Interaction of soil filamentous fungi affects needle composition and nutrition of Norway spruce seedlings

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

The effects of the interactions of soil filamentous fungi (including saprotrophic, mycorrhizal and endophytic fungi) on several morphological and physiological parameters of Norway spruce seedlings [Picea abies (L.) Karst.] were studied in a pot experiment. Both mycorrhizal variants (Hebeloma bryogenes and Cadophora finlandica) were slightly inhibited with respect to the accumulation of aboveground biomass. However, these variants exhibited significantly improved foliar content of N, P, and Ca (H. bryogenes variant also K), compared to controls. The presence of the saprotrophic fungus Setulipes androsaceus attenuated the positive effect of mycorrhizal fungi on Ca, P, and K content, but did not reduce the positive effect of mycorrhizal fungi on the N content of the seedlings’ needles. Raman spectroscopy revealed that both mycorrhizal fungi increased the foliar content of carotenoids compared to the controls, but the effect diminished in the presence of S. androsaceus. In contrast, in the presence of the dark septate endophyte Phialocephala fortinii, needles exhibited significantly higher wax content and lower carotenoid content compared to the mycorrhizal variants. The presence of the saprotrophic isolate Serpula himantoides resulted in a decrease in needle waxes in comparison to controls. The needles’ carotenoid concentration was positively correlated with the levels of needle nutrients (N, P, K, Ca, Mg), while correlation of needle nutrients (N, P) with the needle wax concentration was negative. We conclude that not only individual fungi but also their interactions profoundly affect the nutrition and needle composition of Norway spruce seedlings.

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

Similar content being viewed by others

References

  • Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13. doi:10.1139/b04-171

    Article  Google Scholar 

  • Baar J, Stanton NL (2000) Ectomycorrhizal fungi challenged by saprotrophic basidiomycetes and soil microfungi under different ammonium regimes in vitro. Mycol Res 104:691–697. doi:10.1017/S0953756299002257

    Article  Google Scholar 

  • Bending GD (2003) Litter decomposition, ectomycorrhizal roots and the ‘Gadgil’ effect. New Phytol 158:227–238. doi:10.1046/j.1469-8137.2003.00752.x

    Article  Google Scholar 

  • Boddy L (1999) Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91:13–32. doi:10.2307/3761190

    Article  Google Scholar 

  • Cairney JWG (2005) Basidiomycete mycelia in forest soils: dimensions, dynamics and roles in nutrient distribution. Mycol Res 109:7–20. doi:10.1017/S0953756204001753

    Article  PubMed  Google Scholar 

  • Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740. doi:10.1046/j.1351-0754.2003.0555.x

    Article  Google Scholar 

  • Chandler JW, Dale JE (1995) Nitrogen deficiency and fertilization effects on needle growth and photosynthesis in Sitka spruce (Picea sitchensis). Tree Physiol 15:813–817

    Google Scholar 

  • Conjeaud C, Schreromm P, Muosain D (1996) Effect of ectomycorrhiza and phosphorus on maritime pine seedlings (Pinus pinaster). New Phytol 133:345–351. doi:10.1111/j.1469-8137.1996.tb01901.x

    Article  Google Scholar 

  • Corrêa A, Strasser RJ, Martins-Loução MA (2006) Are Mycorrhiza always beneficial? Plant Soil 279:65–73. doi:10.1007/s11104-005-7460-1

    Article  Google Scholar 

  • Davies FT Jr, Svenson SE, Cole JC, Phavaphutanon L, Duray SA, Olalde-Portugal V, Meier CE, Bo SH (1996) Non-nutritional stress acclimation of mycorrhizal woody plants exposed to drought. Tree Physiol 16:985–993

    Google Scholar 

  • Dosskey MG, Boersma L, Linderman RG (1991) Role for the photosynthate demand of ectomycorrhizas in the response of douglas fir seedlings to drying soil. New Phytol 117:327–334. doi:10.1111/j.1469-8137.1991.tb04914.x

    Article  Google Scholar 

  • Flykt E, Timonen S, Pennanen T (2008) Variation ectomycorrhizal colonisation Norway spruce seedlings in Finnish forest Nurseries. Silva Fenn 42:571–585

    Google Scholar 

  • Gadgil RL, Gadgil PD (1975) Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. N Z J For Sci 5:33–41

    Google Scholar 

  • Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791–795. doi:10.1046/j.1469-8137.2002.00417.x

    Article  Google Scholar 

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91. doi:10.1007/s00572-006-0094-1

    Article  PubMed  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–585. doi:10.1046/j.1469-8137.1997.00729.x

    Article  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310. doi:10.1046/j.1469-8137.1998.00265.x

    Article  Google Scholar 

  • Kaldorf M, Renker C, Fladung M, Buscot F (2004) Characterization and spatial distribution of ectomycorrhizas colonizing aspen clones released in an experimental field. Mycorrhiza 14:295–306. doi:10.1007/s00572-003-0266-1

    Article  PubMed  Google Scholar 

  • Kirchgessner HD, Reichert K, Hauff K, Steinbrecher R, Schnitzler JP, Pfündel EE (2003) Light and temperature, but not UV radiation, affect chlorophylls and carotenoids in Norway spruce needles (Picea abies (L.) Karst.). Plant Cell Environ 26:1169–1179. doi:10.1046/j.1365-3040.2003.01043.x

    Article  CAS  Google Scholar 

  • Klimo E, Hager H, Kulhavý J (2000) Spruce monocultures in Central Europe—problems and prospects. EFI Proc 33:1–208

    Google Scholar 

  • Lindahl BD (2001) Nutrient cycling in boreal forests—a mycological perspective. Studies on phosphorus translocation within and between mycelia of saprotrophic- and mycorrhizal fungi. PhD Thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden

  • 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. doi:10.1046/j.1469-8137.1999.00502.x

    Article  CAS  Google Scholar 

  • Lindahl B, Stenlid J, Finlay RD (2001) Effects of resource availability on mycelial interactions and 32P transfer between a saprotrophic and an ectomycorrhizal fungus in soil microcosms. FEMS Microbiol Ecol 38:43–52. doi:10.1111/j.1574-6941.2001.tb00880.x

    Article  CAS  Google Scholar 

  • Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620. doi:10.1111/j.1469-8137.2006.01936.x

    Article  PubMed  CAS  Google Scholar 

  • Lindblad I (1998) Wood-inhabiting fungi on fallen logs of Norway spruce: relations to forest management and substrate quality. Nord J Bot 18:243–256. doi:10.1111/j.1756-1051.1998.tb01877.x

    Article  Google Scholar 

  • Martin F, Tagu D (1999) Developmental biology of a plant–fungus symbiosis: the ectomycorrhiza. In: Varma A, Hock B (eds) Mycorrhiza, 2nd edn. Springer, Heidelberg, pp 51–73

  • Matějka P, Plešerová L, Budínová G, Havířová K, Mulet X, Skácel F, Volka K (2001) Vibrational biospectroscopy: what can we say about the surface wax layer of Norway spruce needles? J Mol Struct 565–566:305–310. doi:10.1016/S0022-2860(00)00929-7

    Article  Google Scholar 

  • Moore PD, Chapman SB (eds) (1986) Methods in plant ecology. Blackwell, Oxford, pp 604

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. doi:10.1016/S0003-2670(00)88444-5

    Article  CAS  Google Scholar 

  • Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974. doi:10.1007/s11284-007-0390-z

    Article  Google Scholar 

  • Persson T, Bååth E, Clarholm M, Lundkvist H, Söderström B, Sohlenius B (1980) Trophic structure, biomass dynamics and carbon metabolism of soil organisms in a Scots pine forest. Ecol Bull Stockh 32:419–462

    CAS  Google Scholar 

  • Polle A, Mössnang M, von Schönborn A, Sladkovic R, Rennenberg H (1992) Field studies on Norway spruce trees at high altitudes. I. Mineral, pigment and soluble protein contents of needles as affected by climate and pollution. New Phytol 121:89–99. doi:10.1111/j.1469-8137.1992.tb01096.x

    Article  CAS  Google Scholar 

  • Prior S, Pritchard SG, Runion GB, Rogers HH, Mitchell RJ (1997) Influence of atmospheric CO2 enrichment, soil N, and water stress on needle surface wax formation in Pinus palustris (Pinaceae). Am J Bot 84:1070–1077. doi:10.2307/2446150

    Article  Google Scholar 

  • Robinson DC, Wellburn AR (1991) Seasonal changes in the pigments of Norway spruce, Picea abies (L.) Karst, and the influence of summer ozone exposures. New Phytol 119:251–259. doi:10.1111/j.1469-8137.1991.tb01028.x

    Article  CAS  Google Scholar 

  • Senn-Irlet B, Bieri G (1999) Sporocarp succession of soil-inhabiting macrofungi in an autochthonous subalpine Norway spruce forest of Switzerland. For Ecol Manage 124:169–175. doi:10.1016/S0378-1127(99)00064-X

    Article  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 contorta). Mycol Res 99:159–165. doi:10.1016/S0953-7562(09)80880-0

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London, pp 605

  • Solberg S, Rindal TK, Ogner G (1998) Pigment composition in Norway spruce needles suffering from different types of nutrient deficiency. Trees (Berl) 12:289–292. doi:10.1007/s004680050153

    Article  Google Scholar 

  • Trocha LK, Rudawska M, Leski T, Dabert M (2006) Genetic diversity of naturally established ectomycorrhizal fungi on Norway spruce seedlings under nursery conditions. Microb Ecol 52:418–425. doi:10.1007/s00248-006-9110-4

    Article  PubMed  CAS  Google Scholar 

  • Villareal-Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192. doi:10.1111/j.1469-8137.2004.01167.x

    Article  Google Scholar 

  • Vodnik D, Gogala N (1994) Seasonal fluctuations of photosynthesis and its pigments in 1-year mycorrhized spruce seedlings. Mycorrhiza 4:277–281. doi:10.1007/BF00206777

    Article  Google Scholar 

  • Vrålstad T, Schumacher T, Taylor AFS (2002) Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol 153:143–152. doi:10.1046/j.0028-646X.2001.00290.x

    Article  Google Scholar 

  • Wallander H, Lindahl BD, Nilsson LO (2006) Limited transfer of nitrogen between wood decomposing and ectomycorrhizal mycelia when studied in the field. Mycorrhiza 16:213–217. doi:10.1007/s00572-006-0037-x

    Article  PubMed  CAS  Google Scholar 

  • Watanabe FS, Olsen SR (1965) Test of ascorbic acid method for determining phosphates in water and sodium bicarbonate extract from soils. Soil Sci Soc Am Proc 29:677–680

    CAS  Google Scholar 

  • Wu T, Sharda JN, Koide RT (2003) Exploring interactions between saprotrophic microbes and ectomycorrhizal fungi using a protein–tannin complex as an N source by red pine (Pinus resinosa). New Phytol 159:131–139. doi:10.1046/j.1469-8137.2003.00800.x

    Article  CAS  Google Scholar 

  • Zbíral J (1995) Soil analyses I, Czech Central Institute for Supervising and Testing in Agriculture, Brno (in Czech), pp 197

  • Zhu YG, Christie P, Laidlaw AS (2001) Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42:193–199. doi:10.1016/S0045-6535(00)00125-9

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

Financial support from the Grant Agency of the Czech Republic (grants GA203/05/0697 and GA206/05/0269), the Ministry of Education, Youth and Sports of the Czech Republic (grant MSM 6046137307 and Grant Agency of the Academy of Sciences of the Czech Republic (grant AV0Z60050516) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Mycorrhizal Symbioses, Institute of Botany, Academy of Sciences of the Czech Republic, Zámek 1, 252 43, Průhonice, Czech Republic

    Libor Mrnka & Miroslav Vosátka

  2. Department of Analytical Chemistry, Institute of Chemical Technology Prague, Technická 5, 166 28, Prague, Dejvice, Czech Republic

    Helena Tokárová & Pavel Matějka

  3. Department of Mycorrhizal Symbioses, Institute of Botany, Academy of Sciences of the Czech Republic, Lesní 322, 252 43, Průhonice, Czech Republic

    Libor Mrnka

Authors
  1. Libor Mrnka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Helena Tokárová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miroslav Vosátka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pavel Matějka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Libor Mrnka.

Additional information

Communicated by R. Hampp.

Electronic supplementary material

Below is the link to the electronic supplementary material.

468_2009_330_MOESM1_ESM.jpg

Spruce seedlings’ root tip cross-sections (stained by aniline blue): a, b, root tips of seedlings inoculated by Hebeloma bryogenes (M2 and M2S variants) with developed ectomycorrhizal symbiosis (red arrow marks hyphal mantle and red arrowheads mark Hartig net); c, d, root tips of seedlings inoculated by Cadophora finlandica (E2 and E2S variants) with developed ectomycorrhizal symbiosis (red arrow marks hyphal mantle and red arrowheads mark Hartig net); e, f, root tips of seedlings inoculated by Phialocephala fortinii (E1 and E1S variants) developed DSE association (dashed red arrows mark sclerotia, red arrowheads mark intercellular hyphae and doubled red arrows mark intracellular hyphae). Scale = 20 μm (JPG 1374 kb)

468_2009_330_MOESM2_ESM.jpg

Selected Raman spectra measured for the needles of Norway spruce seedlings. Four major bands are indicated, corresponding to water, waxes and carotenoids. Needle cuticular waxes are characterized by bands corresponding to the aliphatic moiety (bands at 2882, 2845 and about 1456 cm-1). Two bands at about 1530 and 1160 cm-1 correspond to the carotenoids, while the relatively weak but broad band at 3220 cm-1 is attributable to the water stretching vibration modes. Spectra of mycorrhizal (M2-1v-A), endophytic (E1-6v-B) and saprotrophic (M1-3v-B) variants are shown (JPG 559 kb)

468_2009_330_MOESM3_ESM.jpg

Intensity (peak area) of C-H Raman spectral bands corresponding to spruce needle waxes. The intensities of experimental variants were derived from individual measured spectra and averaged per pot. Data are expressed as mean ± S.E.M (n=6). Experimental variants: K, control; S, S. androsaceus; M1, S. himantoides; E1, P. fortinii; E2, C. finlandica; XS, variant with the simultaneous presence of X and S. androsaceus. Different letters denote significant differences (p<0.05) for Fungal factor I (letters above brackets) and separately for variants with the absence or the presence of S. androsaceus (letters started by p or x, respectively) (JPG 960 kb)

468_2009_330_MOESM4_ESM.jpg

Intensity (peak area) of C=C Raman spectral band corresponding to spruce needle carotenoids. The intensities of experimental variants were derived from individual measured spectra and averaged per pot. Data are expressed as mean ± S.E.M (n=6). Experimental variants: K, control; S, S. androsaceus; M1, S. himantoides; E1, P. fortinii; E2, C. finlandica; XS, variant with the simultaneous presence of X and S. androsaceus. Different letters denote significant differences (p<0.05) for Fungal factor I (letters above brackets) and separately for variants with the absence or the presence of S. androsaceus (letters started by p or x, respectively) (JPG 751 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mrnka, L., Tokárová, H., Vosátka, M. et al. Interaction of soil filamentous fungi affects needle composition and nutrition of Norway spruce seedlings. Trees 23, 887–897 (2009). https://doi.org/10.1007/s00468-009-0330-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-009-0330-3

Keywords

Search

Navigation