Skip to main content

Advertisement

SpringerLink
Log in

Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations

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

Abstract

The oil sand industry in northeastern Alberta produces vast areas of severely disturbed land. The sodicity of these anthropic soils is one of the principal constraints that impede their revegetation. Previous in vitro studies have shown that the ectomycorrhizal fungi Laccaria bicolor (Maire) Orton UAMH 8232 and Hebeloma crustuliniforme (Bull) Quel. UAMH 5247 have certain salt-resistant traits and thus are candidate species for the inoculation of tree seedlings to be outplanted on salt-affected soil. In this study, the in vitro development of these fungi was compared to that of three mycorrhizal fungi [Suillus tomentosus (Kauff.) Sing., Snell and Dick; Hymenoscyphus sp. and Phialocephala sp.] isolated from a sodic site created by Syncrude Canada Ltd. Their growth, osmotica and Na/Cl contents were assessed over a range (0, 50, 100, 200 mM) of NaCl concentrations. After 21 days, the two ascomycetes (Hymenoscyphus sp. and Phialocephala sp.) were shown to be more resistant to the NaCl treatments than the three basidiomycete species. Of the basidiomycetes, L. bicolor was the most sensitive to NaCl stress, while H. crustuliniforme showed greater water stress resistance, and the S. tomentosus isolate exhibited greater Na and Cl filtering capacities and had a better biomass yield over the NaCl gradient tested. Both ascomycetes used mechanisms other than carbohydrate accumulation to palliate NaCl stress. While the Hymenoscyphus isolate accumulated proline in response to NaCl treatments, the darker Phialocephala isolate may have used compounds such as melanin. The basidiomycete species accumulated mainly mannitol and/or proline in response to increasing concentrations of NaCl.

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

  • Arguelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174:217–224

    Article  CAS  PubMed  Google Scholar 

  • Arnholdt-Schmitt B (2004) Stress-induced cell reprogramming. A role for global genome regulation? Plant Physiol 136:2579–2586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell AA, Wheeler MH (1986) Biosynthesis and functions of fungal melanins. Annu Rev Phytopathol 24:411–451

    Article  CAS  Google Scholar 

  • Bois G, Piché Y, Fung M, Khasa DP (2005) Mycorrhizal inoculum potentials of pure reclamation materials and revegetated tailing sands from the Canadian oil sand industry. Mycorrhiza 15:149–158

    Article  CAS  PubMed  Google Scholar 

  • Brady NC, Weil RR (eds) (2002) The nature and properties of soils, 13th edn. Prentice Hall, USA

  • Brown AD, Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J Gen Microbiol 72:589–591

    Article  CAS  PubMed  Google Scholar 

  • Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136

    Article  CAS  Google Scholar 

  • Chen DM, Ellul S, Herdman K, Cairney JWG (2001) Influence of salinity on biomass production by Australian Pisolithus spp. isolates. Mycorrhiza 11:231–236

    Article  CAS  Google Scholar 

  • Clipson NJW, Jennings DH (1992) Dendryphiella salina and Debaryomyces hensenii: models for ecophysical adaptation to salinity by fungi that grow in the sea. Can J Bot 70:2097–2105

    Article  Google Scholar 

  • Coleman MD, Bledsoe CS, Lopushinsky W (1989) Pure culture response of ectomycorrhizal fungi to imposed water stress. Can J Bot 67:29–39

    Article  Google Scholar 

  • Colpaert JV, Vandenkoornhuyse P, Adriaensen K, Vangronsveld J (2000) Genetic variation and heavy metal tolerance in the ectomycorrhizal basidiomycete Suillus luteus. New Phytol 147:367–379

    Article  CAS  Google Scholar 

  • Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703

    Article  CAS  PubMed  Google Scholar 

  • Dixon RK, Rao MV, Garg VK (1993) Salt stress affects in vitro growth and in situ symbioses of ectomycorrhizal fungi. Mycorrhiza 3:63–68

    Article  Google Scholar 

  • Essington ME (ed) (2004) Soil and water chemistry, an integrative approach. CRC, USA

  • Formina MA, Alexander IJ, Colpaert JV, Gadd GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866

    Article  Google Scholar 

  • Gadd GM (1993) Interaction of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • Galinsky EA, Truper HG (1994) Microbial behavior in salt-stressed ecosystems. FEMS Microbiol Rev 15:95–108

    Article  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Hashem AR (1995) The role of mycorrhizal infection in the tolerance of Vaccinium macrocarpon to iron. Mycorrhiza 5:451–454

    Article  Google Scholar 

  • Jennings DH (1983) Some aspect of the physiology and biochemistry of marine fungi. Biol Rev 58:423–459

    Article  CAS  Google Scholar 

  • Jennings DH (1984) Polyol metabolism in fungi. Adv Microb Physiol 25:149–193

    Article  CAS  PubMed  Google Scholar 

  • Jennings DH, Burke RM (1990) Compatible solute—the mycological dimension and their role as physiological buffering agents. New Phytol 116:277–283

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jumpponen A (1999) Spatial distribution of discrete RAPD phenotypes of a root endophytic fungus, Phialocephala fortinii, at a primary successional site on a glacier forefront. New Phytol 141:333–344

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265

    Article  CAS  PubMed  Google Scholar 

  • Kernaghan G, Hambling B, Fung M, Khasa D (2002) In vitro selection of Boreal ectomycorrhizal fungi for use in reclamation of saline–alkaline habitats. Restor Ecol 10:1–9

    Article  Google Scholar 

  • Kottke I (1992) Ectomycorrhizas—organs for uptake and filtering of cations. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB, Wallingford, UK, pp 316–322

    Google Scholar 

  • Kropp BR, Langlois C-G (1990) Ectomycorrhizae in reforestation. Can J For Res 20:438–451

    Article  Google Scholar 

  • Lerner HR (1999) Introduction to the response of plants to environmental stresses. In: Lerner HR (ed) Plant response to environmental stresses, from phytohormones to genome reorganization. Marcel Dekker, Basel, NY, USA, pp 1–26

    Google Scholar 

  • Levitt J (1980) Response of plants to environmental stresses—water, radiation, salt and other stresses, 2nd edn. Academic, London, UK

  • Lewis DH, Harley JL (1965) Carbohydrate physiology of mycorrhizal roots of beech. I. Identity of endogenous sugars and utilization of exogenous sugars. New Phytol 64:224–237

    Article  CAS  Google Scholar 

  • Lewis DH, Smith DC (1967) Sugar alcohols (Polyols) in fungi and green plants. I. Distribution, physiology and metabolism. New Phytol 66:143–184

    Article  CAS  Google Scholar 

  • Luard EJ (1985) Interaction of substrate C:N ratio and osmotic potential on growth and osmoregulation of four filamentous fungi. New Phytol 101:117–132

    Article  CAS  Google Scholar 

  • Malajczuk N, Reddell P, Brundrett M (1994) Role of ectomycorrhizal fungi in mineland reclamation. In: Pfleger FL, Linderman RG (eds) Mycorrhizae and plant health. APS Press, St. Paul, USA, pp 83–100

    Google Scholar 

  • Mansour MMF, Salama KHA (2004) Cellular basis of salinity tolerance in plants. Environ Exp Bot (in press)

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    Article  CAS  Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of fine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163

    Google Scholar 

  • Mushin TM, Zwiazek JJ (2002) Colonization with Hebeloma crustuliniforme increases water conductance and limits shoot sodium uptake in white spruce (Picea glauca) seedlings. Plant Soil 238:217–225

    Article  Google Scholar 

  • Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu DK, Wang MG, Wang YF (1997) Plant cellular osmotica. Acta Biotheor 45:161–169

    Article  Google Scholar 

  • Paquin R, Lechasseur P (1979) Observations sur une méthode de dosage de la proline libre dans les extraits des plantes. Can J Bot 57:1851–1854

    Article  CAS  Google Scholar 

  • Pfleger FL, Stewart EL, Noyd RK (1994) Role of VAM fungi in mine land revegetation. In: Pfleger FL, Linderman RG (eds) Mycorrhizae and plant health. APS, St. Paul, USA, pp 83–100

    Google Scholar 

  • Pfyffer GE, Rast DM (1988) The polyol pattern of fungi as influenced by the carbohydrate nutrient source. New Phytol 109:321–326

    Article  CAS  Google Scholar 

  • Posas F, Chambers JR, Heyman JA, Hoeffler JP, Nadal E, Arino J (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275:17249–17255

    Article  CAS  PubMed  Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391

    Article  Google Scholar 

  • Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374

    Article  CAS  Google Scholar 

  • Read DJ, Kerley S (1995) The status and function of ericoid mycorrhizal systems. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and technology. Springer, Berlin Heidelberg New York, pp 499–520

    Chapter  Google Scholar 

  • Segner H, Braunbeck T (1998) Cellular response profile to chemical stress. In: Schüürmann G, Market B (eds) Ecotoxicology. Ecological fundamentals, chemical exposure, and biological effects. Wiley, New York, USA, pp 520–569

    Google Scholar 

  • Sharples JM, Chambers SM, Meharg AA, Cairney JWG (2000) Genetic diversity of root-associated fungal endophytes from Calluna vulgaris at contrasting field sites. New Phytol 148:153–162

    Article  CAS  Google Scholar 

  • Shen B, Hohmann S, Jensen RG, Bohnert HJ (1999) Roles of sugar alcohols in osmotic stress adaptation. Replacement of glycerol by mannitol and sorbitol in yeast. Plant Physiol 121:45–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sigler L, Flis A (1998) University of Alberta microfungus collection and herbarium catalogue of strains, 3rd edn. University of Alberta microfungus collection and herbarium (http://www.devonian.ualberta.ca/uamh/), Edmonton, Alberta, Canada

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, San Diego, USA

  • Söderström B, Finlay RD, Read DJ (1988) The structure and function of the vegetative mycelium of ectomycorrhizal plants. IV. Qualitative analysis of carbohydrates contents of mycelium interconnecting host plants. New Phytol 109:163–166

    Article  Google Scholar 

  • Souto C, Pellissier F, Chiapusio G (2000) Allelopathic effects of humus phenolics on growth and respiration of mycorrhizal fungi. J Chem Ecol 26:2015–2023

    Article  CAS  Google Scholar 

  • Sun Y-P, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay R (1999) Exudation–reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms. Mycorrhiza 9:137—144

    Article  CAS  Google Scholar 

  • Takagi H, Iwamoto, Nakamori S (1997) Isolation of freeze-tolerant laboratory strains of Saccharomyces cerevisiae from proline-analogue-resistant mutants. Appl Microbiol Biotechnol 47:405–411

    Article  CAS  PubMed  Google Scholar 

  • Tibbett M, Sanders FE, Cairney JWG (2002) Low-temperature-induced changes in trehalose, mannitol and arabitol associated with enhanced tolerance to freezing in ectomycorrhizal basidiomycetes (Hebeloma spp.). Mycorrhiza 12:249–255

    Article  CAS  PubMed  Google Scholar 

  • Unestam T, Sun Y-P (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5:301–311

    Article  Google Scholar 

  • Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhizia bicolorata—the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate. New Phytol 145:549–563

    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

    Article  Google Scholar 

  • Wiemken A (1990) Trehalose in yeast, stress protectant rather than reserve carbohydrate. J Gen Microbiol 58:209–217

    CAS  Google Scholar 

  • Yeo AR (1983) Salinity resistance: physiologies and prices. Physiol Plant 58:214–222

    Article  CAS  Google Scholar 

  • Yeo A (1998) Molecular biology of salt tolerance in the context of whole-plant physiology. J Exp Bot 49:915–929

    CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by Syncrude Canada Ltd. and NSERC (CRDPJ 250448-01 to D.P. Khasa). We would like to thank Henk den Bakker for valuable help with the phylogenetic analyses of the Suillus and Hymenoscyphus isolates, Alain Brousseau for mineral analyses (Centre de Recherche en Biologie Forestière, Univ. Laval, Canada), and Lucette Chouinard and Pierre Lechasseur for biochemical analyses (Agriculture and Agri-Food Canada). Furthermore, we wish to thank Andrew Coughlan and Jean-Luc Jany for helpful comments and manuscript revision, and Michèle Bernier-Cardou (Laurentian Forestry Center, Canada).

Author information

Authors and Affiliations

  1. Centre de Recherche en Biologie Forestière, Pavillon C.-E.-Marchand, Université Laval, G1K 7P4, Québec (Québec), Canada

    G. Bois, Y. Piché & D. P. Khasa

  2. Soils and Crops Research and Development Centre, Agriculture and Agri-Food Canada, 2560 Blvd. Hochelaga, G1V 2J3, Sainte-Foy (Québec), Canada

    A. Bertrand

  3. Syncrude Canada Ltd., Environmental Affairs Department, P.O. Bag 4009, M.D. 0078, T9H 3L1, Fort McMurray (Alberta), Canada

    M. Fung

  4. Laboratoire de mycologie, local 2110, Pavillon C.-E.-Marchand, Université Laval, G1K 7P4, Québec (Québec), Canada

    G. Bois

Authors
  1. G. Bois
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Bertrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Piché
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Fung
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. P. Khasa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Bois.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bois, G., Bertrand, A., Piché, Y. et al. Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations. Mycorrhiza 16, 99–109 (2006). https://doi.org/10.1007/s00572-005-0020-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-005-0020-y

Keywords

Search

Navigation