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.
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
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
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plant. New Phytol 154:275–304
Burgeff H (1932) Saprophytismus und symbiose. Gustav Fisher, Jena
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
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
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
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
Frankland JC, Poskitt JM, Howard DM (1994) Spatial development of populations of a decomposer fungus, Mycena galopus. Can J Bot 73:S1399–S1406
Freudenstein JV, Broe MB, Feldenkris ER (2016) Phylogenetic relationships at the base of Ericaceae: implications for vegetative and mycorrhizal evolution. Taxon 65:794–804
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
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
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
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
Katoh KS, Daron M (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780
Kernaghan G, Patriquin G (2011) Host associations between fungal root endophytes and boreal trees. Microb Ecol 62:460–473
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
Koide RT, Shardy JN, Herr JR, Malcomm GM (2008) Ectomycorrhizal fungi and the biotrophy–saprotrophy continuum. New Phytol 178:230–233
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
Kron KA, Judd WS, Stevens PF et al (2002) Phylogenetic classification of Ericaceae: Molecular and morphological evidence. Bot Rev 68:335–423
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
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
Márquez SS, Bills GF, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195
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
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
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
Mckeen WE, Smith R, Bhattachaarya PK (1969) Alterations of host wall surrounding infection peg of powdery mildew fungi. Can J Bot 47:701–706
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
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
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
Selosse MA, Setaro S, Glatard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier, Oxford
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
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
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
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
Vasiliauskas R, Menkis A, Finlay RD, Stenlid J (2007) Wood-decay fungi in living roots of conifer seedlings. New Phytol 174:441–446
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
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
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
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
Zhang Y-H, Zhuang W-Y (2004) Phylogenetic relationships of some members in the genus Hymenoscyphus (Ascomycetes, Helotiales ). Nova Hedwigia 78:475–484
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.
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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
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DOI: https://doi.org/10.1007/s00572-017-0797-5