Skip to main content
Log in

A plant growth-promoting symbiosis between Mycena galopus and Vaccinium corymbosum seedlings

  • Short Note
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Typically, Mycena species are viewed as saprotrophic fungi. However, numerous detections of Mycena spp. in the roots of green plants suggest that a continuum from saprotrophy to biotrophy could exist. In particular, mycenoid species have repeatedly been found in Ericaceae plant roots. Our study asked whether (1) Mycena species are commonly found in the roots of green Ericaceae plants; (2) Mycena sequences are limited to a single group/lineage within the genus; and (3) a Mycena sp. can behave as a beneficial root associate with a typical ericoid mycorrhizal plant (Vaccinium corymbosum), regardless of how much external labile carbon is available. We detected Mycena sequences in roots of all sampled Ericaceae plants. Our Mycena sequences clustered in four different groups distributed across the Mycena genus. Only one group could be assigned with confidence to a named species (M. galopus). Our Mycena sequences clustered with other Mycena sequences detected in roots of ericoid mycorrhizal plant species collected throughout Europe, America, and Australia. An isolate of M. galopus promoted growth of V. corymbosum seedlings in vitro regardless of external carbon supply in the media. Seedlings inoculated with M. galopus grew as well as those inoculated with the ericoid mycorrhizal fungus Rhizoscyphus ericae. Surprisingly, this M. galopus isolate colonized Vaccinium roots and formed distinctive peg-like structures. Our results suggest that Mycena species might operate along a saprotroph–symbiotic continuum with a range of ericoid mycorrhizal plant species. We discuss our results in terms of fungal partner recruitment by Ericaceae plants.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Bougoure DS, Cairney JWG (2005) Assemblages of ericoid mycorrhizal and other root-associated fungi from Epacris pulchella (Ericaceae) as determined by culturing and direct DNA extraction from roots. Environ Microbiol 7:819–827

    Article  CAS  PubMed  Google Scholar 

  • Bougoure DS, Parkin PI, Cairney JWG, Alexander IJ, Anderson IC (2007) Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Mol Ecol 16:4624–4636

    Article  CAS  PubMed  Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plant. New Phytol 154:275–304

    Article  Google Scholar 

  • Burgeff H (1932) Saprophytismus und symbiose. Gustav Fisher, Jena

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Curlevski NJA, Chambers SM, Anderson IC, Cairney JWG (2009) Identical genotypes of an ericoid mycorrhiza-forming fungus occur in roots of Epacris pulchella (Ericaceae) and Leptospermum polygalifolium (Myrtaceae) in an Australian sclerophyll forest. FEMS Microbiol Ecol 67:411–420

    Article  CAS  PubMed  Google Scholar 

  • Davey ML, Heimdal R, Ohlson M, Kauserud H (2013) Host- and tissue-specificity of moss-associated Galerina and Mycena determined from amplicon pyrosequencing data. Fungal Ecol 6:179–186

    Article  Google Scholar 

  • Emmett EE, Aronsen A, Læssøe T, Elborne SA (2008) Mycena (Pers.) Roussel. In: Knudsen H, Vesterholt J (eds) Funga Nordica: Agaricoid, Boletoid, and Cyphelloid genera. Nordsvamp, Copenhagen, p 352e387

    Google Scholar 

  • Frankland JC, Poskitt JM, Howard DM (1994) Spatial development of populations of a decomposer fungus, Mycena galopus. Can J Bot 73:S1399–S1406

    Article  Google Scholar 

  • Freudenstein JV, Broe MB, Feldenkris ER (2016) Phylogenetic relationships at the base of Ericaceae: implications for vegetative and mycorrhizal evolution. Taxon 65:794–804

    Article  Google Scholar 

  • Grelet GA, Johnson D, Paterson E, Anderson IC, Alexander IJ (2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182:359–366

    Article  CAS  PubMed  Google Scholar 

  • Grelet GA, Johnson D, Vrålstad T, Alexander IJ, Anderson IC (2010) New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytol 188:210–222

    Article  CAS  PubMed  Google Scholar 

  • Grelet GA, Martino E, Dickie IA, Tajuddin R, Artz RAA (2016) Ecology of ericoid mycorrhizal fungi: what insight have we gained with molecular tools and what’s missing? In: Martin F (ed) Molecular mycorrhizal Symbiosis. Springer, p 405-419

  • Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508

    Article  CAS  PubMed  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 

  • Katoh KS, Daron M (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kernaghan G, Patriquin G (2011) Host associations between fungal root endophytes and boreal trees. Microb Ecol 62:460–473

    Article  PubMed  Google Scholar 

  • Kjøller R, Olsrud M, Michelsen A (2010) Co-existing ericaceous plant species in a subarctic mire community share fungal root endophytes. Fungal Ecol 3:205–214

    Article  Google Scholar 

  • Koide RT, Shardy JN, Herr JR, Malcomm GM (2008) Ectomycorrhizal fungi and the biotrophy–saprotrophy continuum. New Phytol 178:230–233

    Article  PubMed  Google Scholar 

  • Kosola KR, Workmaster BAA, Spada PA (2007) Inoculation of cranberry (Vaccinium macrocarpon) with the ericoid mycorrhizal fungus Rhizoscyphus ericae increases nitrate influx. New Phytol 176:184–196

    Article  PubMed  Google Scholar 

  • Kron KA, Judd WS, Stevens PF et al (2002) Phylogenetic classification of Ericaceae: Molecular and morphological evidence. Bot Rev 68:335–423

    Article  Google Scholar 

  • Lallemand F, Gaudeul M, Lambourdière J, Matsuda Y, Hashimoto Y, Selosse M-A (2016) The elusive predisposition to mycoheterotrophy in Ericaceae. New Phytol 212:314–319

    Article  PubMed  Google Scholar 

  • Lorberau KE, Botnen SS, Mundra S, Aas AB, Rozema J, Eidesen PB, Kauserud H (2017) Does warming by open-top chambers induce change in the root-associated fungal community of the arctic dwarf shrub Cassiope tetragona (Ericaceae)? Mycorrhiza 27:513–524

    Article  PubMed  Google Scholar 

  • Márquez SS, Bills GF, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195

    Google Scholar 

  • Martino E, Morin E, Grelet GA et al (2017) Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. Submitted to New Phytol

  • Martos F, Dulormne M, Pailler T, Bonfante P, Faccio A, Fournel J, Dubois M-P, Selosse M-A (2009) Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytol 184:668–681

    Article  CAS  PubMed  Google Scholar 

  • Marx DH, Bryan WC (1975) Growth and ectomycorrhizal development of loblolly pine seedlings in fumigated soil infected with the fungal symbiont Pisolithus tinctorius. For Sci 21:245–254

    Article  Google Scholar 

  • Massicotte HB, Melville LH, Peterson RL (2005) Structural features of mycorrhizal associations in two members of the Monotropoideae, Monotropa uniflora and Pterospora andromedea. Mycorrhiza 15:101–110

    Article  CAS  PubMed  Google Scholar 

  • Mckeen WE, Smith R, Bhattachaarya PK (1969) Alterations of host wall surrounding infection peg of powdery mildew fungi. Can J Bot 47:701–706

    Article  Google Scholar 

  • Nilsson RH, Abarenkov K, Veldre V, Nylinder S, DE Wit P, Brosché S, Alfredsson JF, Ryberg M, Kristiansson E (2010) An open source chimera checker for the fungal ITS region. Mol Ecol Resour 10:1076–1081

    Article  CAS  PubMed  Google Scholar 

  • Ogura-Tsujita Y, Gebauer G, Hashimoto T, Umata H, Yukawa Y (2009) Evidence for novel and specialized mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proc Biol Sci B 276:761–767

    Article  CAS  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07-0. http://www.R-project.org

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

  • Selosse MA, Cameron DD (2010) Introduction to a virtual special issue on mycoheterotrophy: new phytologist sheds light on non-green plants. New Phytol 185:591–593

    Article  PubMed  Google Scholar 

  • Selosse MA, Setaro S, Glatard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier, Oxford

    Google Scholar 

  • Smith GR, Finlay RD, Stenlid J, Vasaitis R, Menkis A (2017) Growing evidence for facultative biotrophy in saprotrophic fungi: data from microcosm tests with 201 species of wood-decay basidiomycetes. New Phytol 215:747–755

  • Suetsugu K, Yamato M, Miura C, Yamaguchi K, Takahashi K, Ida Y, Shigenobu S, Kaminaka H (2017) Comparison of green and albino individuals of the partially mycoheterotrophic orchid Epipactis helleborine on molecular identities of mycorrhizal fungi, nutritional modes and gene expression in mycorrhizal roots. Mol Ecol 26:1652–1669. doi:10.1111/mec.14021

    Article  CAS  PubMed  Google Scholar 

  • Tejesvi MV, Sauvola T, Pirttilä AM, Ruotsalainen AL (2013) Neighboring Deschampsia flexuosa and Trientalis europaea harbor contrasting root fungal endophytic communities. Mycorrhiza 23:1–10

    Article  PubMed  Google Scholar 

  • Toftegaard T, Iason GR, Alexander IJ et al (2010) The threatened plant intermediate wintergreen (Pyrola media) associates with a wide range of biotrophic fungi in native Scottish pine woods. Biodivers Conserv 19:3963–3971

    Article  Google Scholar 

  • Toju H, Yamamoto S, Sato H, Tanabe AS (2013) Sharing of diverse mycorrhizal and root-endophytic fungi among plant species in an oak-dominated cool–temperate forest. PLoS One 8(10):e78248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasiliauskas R, Menkis A, Finlay RD, Stenlid J (2007) Wood-decay fungi in living roots of conifer seedlings. New Phytol 174:441–446

    Article  CAS  PubMed  Google Scholar 

  • Vohník M, Fendrych M, Kolarik M, Gryndler M, Hrselova H, Albrechtová J, Vosátka M (2007) Intracellular colonization of Rhododendron and Vaccinium roots by Cenococcum geophilum, Geomyces pannorum and Meliniomyces variabilis. Folia Microbiol 52:407–414

    Article  Google Scholar 

  • Vohník M, Sadowsky JJ, Kohout P, Lhotáková Z, Nestby R, Kolarík M (2012a) Novel root-fungus symbiosis in Ericaceae: sheathed ericoid mycorrhiza formed by a hitherto undescribed basidiomycete with affinities to Trechisporales. PLoS One 7(6):e39524. doi:10.1371/journal.pone.0039524

    Article  PubMed  PubMed Central  Google Scholar 

  • Vohník M, Sadowsky JJ, Lukešová T, Albrechtová J, Vosátka M (2012b) 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

    Article  Google Scholar 

  • Wang H, Wang Z, Zhang F, Liu J, He X (1997) A cytological study on the nutrient-uptake mechanism of a saprotrophic orchid Gastrodia elata. Acta Bot Sin 39:500–504

    Google Scholar 

  • Zhang Y-H, Zhuang W-Y (2004) Phylogenetic relationships of some members in the genus Hymenoscyphus (Ascomycetes, Helotiales ). Nova Hedwigia 78:475–484

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Hedda Weitz (University of Aberdeen, UK) and Prof David Read (University of Sheffield, UK) for supplying the cultures of Mycena gallopus and Rhizoscyphus ericae. We are also grateful to Catherine Smart and Alan Sim for technical support and to Melanie Jones for statistical advice. Finally, our thanks go to Prof Ian Alexander, who patiently guided the field collection and provided generous feedbacks on the experimental design and data interpretation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gwen-Aëlle Grelet.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grelet, GA., Ba, R., Goeke, D.F. et al. A plant growth-promoting symbiosis between Mycena galopus and Vaccinium corymbosum seedlings. Mycorrhiza 27, 831–839 (2017). https://doi.org/10.1007/s00572-017-0797-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-017-0797-5

Keywords

Navigation