Skip to main content
SpringerLink
Log in

The influence of the ectomycorrhizal fungus Rhizopogon subareolatus on growth and nutrient element localisation in two varieties of Douglas fir (Pseudotsuga menziesii var. menziesii and var. glauca) in response to manganese stress

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

Abstract

Acidification of forest ecosystems leads to increased plant availability of the micronutrient manganese (Mn), which is toxic when taken up in excess. To investigate whether ectomycorrhizas protect against excessive Mn by improving plant growth and nutrition or by retention of excess Mn in the hyphal mantle, seedlings of two populations of Douglas fir (Pseudotsuga menziesii), two varieties, one being menziesii (DFM) and the other being glauca (DFG), were inoculated with the ectomycorrhizal fungus Rhizopogon subareolatus in sand cultures. Five months after inoculation, half of the inoculated and non-inoculated seedlings were exposed to excess Mn in the nutrient solution for further 5 months. At the end of this period, plant productivity, nutrient concentrations, Mn uptake and subcellular compartmentalisation were evaluated. Non-inoculated, non-stressed DFM plants produced about 2.5 times more biomass than similarly treated DFG. Excess Mn in the nutrient solution led to high accumulation of Mn in needles and roots but only to marginal loss in biomass. Colonisation with R. subareolatus slightly suppressed DFM growth but strongly reduced that of DFG (−50%) despite positive effects of mycorrhizas on plant phosphorus nutrition. Growth reductions of inoculated Douglas fir seedlings were unexpected since the degree of mycorrhization was not high, i.e. ca. 30% in DFM and 8% in DFG. Accumulation of high Mn was not prevented in inoculated seedlings. The hyphal mantle of mycorrhizal root tips accumulated divalent cations such as Ca, but not Mn, thus not providing a barrier against excessive Mn uptake into the plants associated with R. subareolatus.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Álvarez IF, Parladé J, Trappe JM, Castellano MA (1993) Hypogeous mycorrhizal fungi of Spain. Mycotaxon 47:201–217

    Google Scholar 

  • Arines J, Vilarino A, Sainz M (1989) Effect of different inocula of vesicular–arbuscular mycorrhizal fungi on manganese content and concentration in red-clover (Trifolium Pratense L) plants. New Phytol 112:215–219

    Article  Google Scholar 

  • Bâ AM, Sanon KB, Duponnois R, Dexheim J (1999) Growth response of Afzelia africana Sm. seedlings to ectomycorrhizal inoculation in a nutrient-deficient soil. Mycorrhiza 9:91–95

    Article  Google Scholar 

  • Bethlenfalvay GJ, Franson RL (1989) Manganese toxicity alleviated by mycorrhizae in soybean. J Plant Nutr 12:953–970

    Article  CAS  Google Scholar 

  • Blaudez D, Jacob C, Turnau K, Colpaert JV, Ahonen-Jonnarth U, Finlay R, Botton B, Chalot M (2000) Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res 104:1366–1371

    Article  CAS  Google Scholar 

  • Block J (1997) Schadsituation der Douglasie in Rheinland-Pfalz. Stand der Ursachenforschung zu Douglasienschäden-derzeitige Empfehlungen für die Praxis. Mitteilungen der Forstlichen Forschungsanstalt Rheinland-Pfalz 41, Trippstadt, pp 46–75

  • Bücking H, Heyser W (2000) Subcellular compartmentation of elements in non-mycorrhizal and mycorrhizal roots of Pinus sylvestris: an X-ray microanalytical study. I. The distribution of phosphate. New Phytol 145:311–320

    Article  Google Scholar 

  • Burgess T, Dell B, Malajczuk N (1994) Variation in mycorrhizal development and growth stimulation of 20 Pisolithus isolates inoculated onto Eucalyptus grandis W. Hill ex Maiden. New Phytol 127:731–739

    Article  Google Scholar 

  • Cairney JWG, Chambers SM (1997) Interaction between Pisolithus tinctoriusits hosts: a review of current knowledge. Mycorrhiza 7:117–131

    Article  Google Scholar 

  • Cardoso EJBN (1985) Effect of vesicular arbuscular mycorrhiza and rock phosphate on the soybean–Rhizobium symbiosis. Rev Bras Ciênc Solo 9:125–130

    Google Scholar 

  • Castellano MA (1996) Outplanting performance of mycorrhizal inoculated seedlings. In: Mukerji KG (ed) Concepts in mycorrhizal research. Kluwer Academic, Dordrecht, The Netherlands, pp 223–302

    Chapter  Google Scholar 

  • Colpaert JV, Van Assche JA, Luijtens K (1992) The growth of the extramatrical mycelium of ectomycorrhizal fungi and the growth response of Pinus sylvestris L. New Phytol 120:127–135

    Article  Google Scholar 

  • Corrêa A, Strasser RJ, Martins-Loucao MA (2006) Are mycorrhiza always beneficial? Plant Soil 279:65–73

    Article  Google Scholar 

  • Davis FT, Potter JR, Linderman RG (1992) Mycorrhiza and repeated drought exposure affect drought resistance and extraradical hyphae development of pepper plants independent of plant size and nutrient. J Plant Physiol 139:289–294

    Article  Google Scholar 

  • Dosskey M, Boersma L, Linderman RG (1990) Role for photosynthate demand for ectomycorrhizas in the response of Douglas-fir seedlings to drying soil. New Phytol 117:327–334

    Article  Google Scholar 

  • Dučić T, Polle A (2007) Manganese toxicity in two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca) seedlings as affected by phosphorus supply. Funct Plant Biol 34:31–40

    Article  Google Scholar 

  • Dučić T, Leinemann L, Finkeldey R, Polle A (2006) Uptake and translocation of manganese in seedlings of two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca). New Phytol 170:11–20

    Article  PubMed  Google Scholar 

  • Eltrop L, Marschner H (1996) Growth and mineral nutrition of non-mycorrhizal and mycorrhizal Norway spruce (Picea abies) seedlings grown in semi-hydroponic sand culture.1. Growth and mineral nutrient uptake in plants supplied with different forms of nitrogen. New Phytol 133:469–478

    Article  CAS  Google Scholar 

  • Fritz E (1989) X-ray-microanalysis of diffusible elements in plant cells after freeze-drying, pressure-infiltration with ether and embedding in plastic. Scanning Microsc 3:517–526

    CAS  Google Scholar 

  • Fritz E, Jentschke G (1994) Agar standards for quantitative X-ray-microanalysis of resin-embedded plant-tissues. J Microsc 174:47–50

    Article  CAS  Google Scholar 

  • Gadd GM (1992) Interaction of fungi with toxic metals. New Phytol 124:25–60

    Article  Google Scholar 

  • Gafur A, Schutzendubel A, Langenfeld-Heyser R, Fritz E, Polle A (2004) Compatible and incompetent Paxillus involutus isolates for ectomycorrhiza formation in vitro with poplar (Populus × canescens) differ in H2O2 production. Plant Biol 6:91–99

    Article  CAS  PubMed  Google Scholar 

  • Galli U, Schuepp H, Brunhold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92:364–368

    Article  CAS  Google Scholar 

  • Hampp R, Wiese J, Mikolajewski S, Nehls U (1999) Biochemical and molecular aspects of C/N interaction in ectomycorrhizal plants: an update. Plant Soil 215:103–113

    Article  CAS  Google Scholar 

  • Heinrichs H, Brumsack HJ, Loftfield N, Konig N (1986) Improved pressure digestion system for biological and anorganic materials. Z Pflanzenernähr Bodenkd 149:350–353

    Article  CAS  Google Scholar 

  • Ingestad T, Lund AB (1986) Theory and techniques for steady state mineral nutrition and growth of plants. Scand J For Res 1:439–453

    Article  Google Scholar 

  • Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116

    Article  CAS  Google Scholar 

  • Kleinschmit J, Racz J, Weisgerber H, Dietze W, Dieterich H, Dimpflmeier R (1974) Ergebnisse aus dem internationalen Douglasien-Herkunftsversuch von 1970 in der Bundesrepublik Deutschland. Silvae Genet 23:167–176

    Google Scholar 

  • Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol 117:365–386

    Article  CAS  Google Scholar 

  • Kothari SK, Marschner H, Römheld V (1990) Direct and indirect effects of VA mycorrhizal fungi and rhizosphere microorganisms on acquisition of mineral nutrients by maize (Zea mays L) in a calcareous soil. New Phytol 116:637–645

    Article  CAS  Google Scholar 

  • Kothari SK, Marschner H, Römheld V (1991) Contribution of the VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 131:177–185

    Article  CAS  Google Scholar 

  • Kunst L, Roomans GM (1985) Intracellular localization of heavy metals in yeast Saccharomyces cerevisae by X-ray microanalysis. Scan Electron Micros 1:191–199

    Google Scholar 

  • Larsen JB (1978) Investigations on significance of potassium and nitrogen supply for drought hardiness in Douglas fir (Pseudotsuga menziesii) in winter. Flora 167:197–207

    Article  Google Scholar 

  • Larsen JB (1981) Geographic variation in winter drought resistance of Douglas fir (Pseudotsuga menziesii Mirb. Franco). Silvae Genet 30:109–114

    Google Scholar 

  • Liesebach M, Stephan BR (1995) Growth performance and reaction to biotic and abiotic factors of Douglas fir progenies (Pseudotsuga menziesii [Mirb] Franco). Silvae Genet 44:303–311

    Google Scholar 

  • Linnemann G (1960) Rassenunterschiede bei Pseudotsuga taxifolia hinsichtlich der Mycorrhiza. Allg Forst Jagdztg 131:41–48

    Google Scholar 

  • Luoma DL, Stockdale CA, Molina R, Eberhart JL (2006) The spatial influence of Douglas-fir retention trees on ectomycorrhiza diversity. Can J For Res 36:2561–2573

    Article  Google Scholar 

  • Lu X, Malajczuk N, Dell B (1998) Mycorrhiza formation and growth of Eglobulus seedlings inoculated with spores of various ectomycorrhizal fungi. Mycorrhiza 8:81–86

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • Massicotte HB, Molina R, Luoma DL, Smith JE (1994) Biology of the ectomycorrhizal genus, Rhizopogon: II. Patterns of host-fungus specificity following spore inoculation of diverse hosts grown in monoculture and dual culture. New Phytol 126:677–690

    Article  Google Scholar 

  • Molina R, Palmer JG (1982) Isolation, maintance, and pure culture manipulation of ectomycorrhizal fungi. In: Schenck NC (ed) Methods and principles of mycorrhizal research. The American Phytopathological Society, St Paul, Minnesota, pp 115–129

    Google Scholar 

  • Molina R, Trappe JM (1982) Patterns of ectomycorrhizal host specificity and potential among Pacific northwest conifers and fungi. Forest Sci 28:423–458

    Google Scholar 

  • Molina R, Trappe JM (1994) Biology of the ectomycorrhizal genus, Rhizopogon. 1. Host association, host specificity and pure culture synthesis. New Phytol 126:653–675

    Article  Google Scholar 

  • Nilsen P, Borja I, Knutsen H, Brean R (1998) Nitrogen and drought effects on ectomycorrhizae of Norway spruce [Picea abies L. (Karst.)]. Plant Soil 198:179–184

    Article  CAS  Google Scholar 

  • Nogueira MA, Cardoso EJ (2003) Microbial interactions on manganese availability and uptake by soybean. Pesqui Agropecu Bras 37:1605–1612

    Article  Google Scholar 

  • Outerbridge RA, Trofymow JA (2004) Diversity of ectomycorrhizae on experimentally planted Douglas-fir seedlings in variable retention forestry sites on southern Vancouver Island. Can J Bot 82:1671–1681

    Article  Google Scholar 

  • Pacovsky RS (1986) Micronutrient uptake and distribution in mycorrhizal or phosphorus-fertilized soybeans. Plant Soil 95:379–388

    Article  CAS  Google Scholar 

  • Parke JL, Linderman RG, Trappe JM (1983) Effects of forest litter on mycorrhiza development and growth of Douglas-fir and Western Red Cedar seedlings. Can J For Res 13:666–671

    Article  Google Scholar 

  • Parladé J, Álvarez IF, Pera J (1995) Ability of native ectomycorrhizal fungi from northern Spain to colonize Douglas-fir and other introduced conifers. Mycorrhiza 6:51–55

    Article  Google Scholar 

  • Parladé J, Pera J, Álvarez IF, Bouchard D, Genere B, Le Tacon F (1999) Effect of inoculation and substrate disinfection method on rooting and ectomycorrhiza formation of Douglas fir cuttings. Ann For Sci 56:35–40

    Article  Google Scholar 

  • Pera J, Álvarez IF, Rincón A, Parladé J (1999) Field performance in northern Spain of Douglas-fir seedlings inoculated with ectomycorrhizal fungi. Mycorrhiza 9:77–84

    Article  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124

    Article  CAS  Google Scholar 

  • Reid CPP, Kidd FA, Ekwebalam SA (1983) Nitrogen nutrition, photosynthesis and carbon allocation in ectomycorrhizal pine. Plant Soil 71:415–532

    Article  CAS  Google Scholar 

  • Schober R, Kleinschmit J, Svolba J (1983) Results of the Douglas-fir provenances experiment of 1958 in Northern Germany. 1. Allg Forst Jagdztg 154:209–236

    Google Scholar 

  • Schober R, Kleinschmit J, Svolba J (1984) Results of the Douglas-fir provenances experiment of 1958 in Northern Germany. 2. Allg Forst Jagdztg 155:53–80

    Google Scholar 

  • Schöne D (1992) Site- and acid-rain induced nutritional disorders of Douglas-fir in Southwestern Germany. Allg Forst Jagdztg 163:53–59

    Google Scholar 

  • Schroeder MS, Janos DP (2004) Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas. Plant Soil 264:335–348

    Article  CAS  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    PubMed  Google Scholar 

  • Shi LB, Guttenberger M, Kottke I, Hampp R (2002) The effect of drought on mycorrhizas of beech (Fagus sylvatica L.): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza 12:303–311

    Article  CAS  PubMed  Google Scholar 

  • Smith HA, Zeller M (1966) A preliminary account of the North American species of Rhizopogon. Mem N Y Bot Gard 14:1–178

    Google Scholar 

  • St Clair SB, Lynch JP (2004) Photosynthetic and antioxidant enzyme responses of sugar maple and red maple seedlings to excess manganese in contrasting light environments. Funct Plant Biol 31:1005–1014

    Article  Google Scholar 

  • Thomson BD, Grove TS, Malajczuk N, StJ. Hardy G (1994) The effectiveness of ectomycorrhizal fungi in increasing the growth of Eucalyptus globulus Labill in relation to root colonization and hyphal development in soil. New Phytol 126:517–524

    Article  Google Scholar 

  • Trappe JM (1977) Selection of fungi for ectomycorrhizal inoculation in nurseries. Annu Rev Phytopathol 15:203–222

    Article  Google Scholar 

  • Turnau K, Kottke I, Oberwinkler F (1993) Element localization in mycorrhizal roots of Pteridium aquilinum L. Kuhn collected from experimental plots treated with cadmium dust. New Phytol 123:313–324

    Article  CAS  Google Scholar 

  • Van Tichelen KK, Colpaert JV, Van Assche JA (1996) Development of arbuscular mycorrhizas in a heavy metal-contaminated soil amended with a metal immobilizing substance. In: Azcon-Aguilar C, Barea JM (eds) Mycorrhizas in integrated systems: from genes to plant development. European Commission, EUR 16728, Luxembourg, pp 479–482

    Google Scholar 

  • Zarb J, Walters DR (1995) Polyamine biosynthesis in the ectomycorrhizal fungus Paxillus involutus exposed to zinc. Lett Appl Microbiol 21:93–95

    Article  CAS  Google Scholar 

  • Zarb J, Walters DR (1996) Polyamine biosynthesis in the ectomycorrhizal fungus Paxillus involutus exposed to lead. Mycol Res 100:486–488

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to the German Science Foundation (DFG) for financial support (Po362/14). We thank Theres Riemekasten and Mariane Smiatacz for excellent technical assistance. We are grateful to two anonymous reviewers for helpful comments.

Open Access

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Author information

Authors and Affiliations

  1. Institut für Forstbotanik, Georg-August Universität Göttingen, Büsgenweg 2, 37077, Göttingen, Germany

    Tanja Dučić & Andrea Polle

  2. Departament de Protecció Vegetal, Institut de Recerca i Tecnología Agroalimentàries (IRTA), Carretera de Cabrils s/n, 08348, Cabrils, Barcelona, Spain

    Javier Parladé

Authors
  1. Tanja Dučić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Javier Parladé
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrea Polle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Polle.

Appendices

Appendix 1

Table 4 Element concentrations in roots and needles in Douglas fir (Pseudotsuga menziesii) variety menziesii and variety glauca after inoculation with Rhizopogon subareolatus and treatment with 10 mM manganese and after inoculation with R. subareolatus
Full size table

Appendix 2

Table 5 Element concentrations in different subcellular locations in mycorrhizal and non-mycorrhizal root tips of Douglas fir (Pseudotsuga menziesii) variety menziesii (DFM) and variety glauca (DFG)
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dučić, T., Parladé, J. & Polle, A. The influence of the ectomycorrhizal fungus Rhizopogon subareolatus on growth and nutrient element localisation in two varieties of Douglas fir (Pseudotsuga menziesii var. menziesii and var. glauca) in response to manganese stress. Mycorrhiza 18, 227–239 (2008). https://doi.org/10.1007/s00572-008-0174-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-008-0174-5

Keywords

Search

Navigation