Skip to main content
SpringerLink
Log in

First record of Rhizoscyphus ericae in Southern Hemisphere’s Ericaceae

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

Abstract

Ericoid mycorrhiza is arguably the least investigated mycorrhizal type, particularly when related to the number of potential hosts and the ecosystems they inhabit. Little is known about the global distribution of ericoid mycorrhizal (ErM) fungi, and this holds true even for the prominent ErM mycobiont Rhizoscyphus ericae. Earlier studies suggested R. ericae might be low in abundance or absent in the roots of Southern Hemisphere’s Ericaceae, and our previous investigations in two Argentine Patagonian forests supported this view. Here, we revisited the formerly investigated area, albeit at a higher altitude, and screened fungi inhabiting hair roots of Gaultheria caespitosa and Gaultheria pumila at a treeless alpine site using the same methods as previously. We obtained 234 isolates, most of them belonging to Ascomycota. In contrast to previous findings, however, among 37 detected operational taxonomic units (OTUs), OTU 1 (=R. ericae s. str.) comprised the highest number of isolates (87, ∼37 %). Most of the OTUs and isolates belonged to the Helotiales, and 82.5 % of isolates belonged to OTUs shared between both Gaultheria species. At the alpine site, ericoid mycorrhizal fungi dominated, followed by dark septate endophytes and aquatic hyphomycetes probably acting as root endophytes. Our results suggest that the distribution of R. ericae is influenced, among others, by factors related to altitude such as soil type and presence/absence and type of the neighboring vegetation. Our study is the first report on R. ericae colonizing Ericaceae roots in the Southern Hemisphere and extends the known range of this prominent ErM species to NW Patagonia.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson LG, Rocliffe S, Haddaway NR, Dunn AM (2015) The role of tourism and recreation in the spread of non-native species: a systematic review and meta-analysis. PLoS One 10:e0140833

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baba T, Hirose D, Sasaki N, Watanabe N, Kobayashi N, Kurashige Y, Karimi F, Ban T (2016) Mycorrhizal formation and diversity of endophytic fungi in hair roots of Vaccinium oldhamii Miq. in Japan. Microbes Environ 31:186–189

    Article  PubMed  PubMed Central  Google Scholar 

  • Bahram M, Peay KG, Tedersoo L (2015) Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytol 205:1454–1463

    Article  CAS  PubMed  Google Scholar 

  • Baral HO, Krieglsteiner L (2006) Hymenoscyphus subcarneus, a little known bryicolous discomycete found in the Białowieża National Park. Acta Mycol 41:11–20

    Article  Google Scholar 

  • Boddy L (2000) Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiol Ecol 31:185–194

    Article  CAS  PubMed  Google Scholar 

  • Bonfante-Fasolo P (1980) Occurrence of a basidiomycete in living cells of mycorrhizal hair roots of Calluna vulgaris. Trans Br Mycol Soc 75:320–325

    Article  Google Scholar 

  • Borchsenius F (2009) FastGap 1.2. Department of Biosciences, Aarhus University, Denmark. http://www.aubot.dk/FastGap_home.htm

  • Bougoure DS, Cairney JWG (2005a) 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, Cairney JWG (2005b) Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environ Microbiol 7:1743–1754

    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 

  • Brook PL (1952) Mycorrhiza of Pernettya macrostigma. New Phytol 51:388–397

    Article  Google Scholar 

  • Bruzone MC, Fontenla SB, Vohník M (2015) Is the prominent ericoid mycorrhizal fungus Rhizoscyphus ericae absent in the Southern Hemisphere’s Ericaceae? A case study on the diversity of root mycobionts in Gaultheria spp. from northwest Patagonia, Argentina. Mycorrhiza 25:25–40

    Article  PubMed  Google Scholar 

  • Cairney JWG, Ashford AE (2002) Biology of mycorrhizal associations of epacrids (Ericaceae). New Phytol 154:305–326

    Article  Google Scholar 

  • Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740

    Article  Google Scholar 

  • Chambers SM, Williams PG, Seppelt RD, Cairney JWG (1999) Molecular identification of Hymenoscyphus sp. from rhizoids of the leafy liverwort Cephaloziella exiliflora in Australia and Antarctica. Mycol Res 103:286–288

    Article  CAS  Google Scholar 

  • Chambers SM, Liu G, Cairney JWG (2000) ITS rDNA sequence comparison of ericoid mycorrhizal endophytes from Woollsia pungens. Mycol Res 104:168–174

    Article  CAS  Google Scholar 

  • Chaurasia B, Pandey A, Palni LMS (2005) Distribution, colonization and diversity of arbuscular mycorrhizal fungi associated with central Himalayan rhododendrons. Forest Ecol Managem 207:315–324

  • 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 

  • Egger KN, Osmond G, Goodier JL (1995) Sequence and putative secondary structure of group I introns in the nuclear-encoded ribosomal RNA genes of the fungus Hymenoscyphus ericae. Biochim Biophys Acta 1261:275–278

    Article  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Gorzelak MA, Hambleton S, Massicotte HB (2012) Community structure of ericoid mycorrhizas and root-associated fungi of Vaccinium membranaceum across an elevation gradient in the Canadian Rocky Mountains. Fungal Ecol 5:36–45

    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 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Sym Ser 41:95–98

    CAS  Google Scholar 

  • Hambleton S, Currah RS (1997) Fungal endophytes from the roots of alpine and boreal Ericaceae. Can J Bot 75:1570–1581

    Article  Google Scholar 

  • Hambleton S, Huhtinen S, Currah RS (1999) Hymenoscyphus ericae: a new record from western Canada. Mycol Res 103:1391–1397

    Article  Google Scholar 

  • Hazard C, Gosling P, Mitchell DT, Doohan FM, Bending GD (2014) Diversity of fungi associated with hair roots of ericaceous plants is affected by land use. FEMS Microbiol Ecol 87:586–600

    Article  CAS  PubMed  Google Scholar 

  • Hutton BJ, Dixon KW, Sivasithamparam K (1994) Ericoid endophytes of Western-Australian heaths (Epacridaceae). New Phytol 127:557–566

    Article  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 

  • Kerley SJ, Read DJ (1998) The biology of mycorrhiza in the Ericaceae 20. Plant and mycorrhizal necromass as nitrogenous substrates for ericoid mycorrhizal fungus Hymenoscyphus ericae and its host. New Phytol 139:353–360

    Article  Google Scholar 

  • Kernan MJ, Finocchio AF (1983) A new discomycete associated with the roots of Monotropa uniflora (Ericaceae). Mycologia 75:916–920

    Article  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 

  • Kohout P, Sýkorová Z, Bahram M, Hadincová V, Albrechtová J, Tedersoo L, Vohník M (2011) Ericaceous dwarf shrubs affect ectomycorrhizal fungal community of the invasive Pinus strobus and native Pinus sylvestris in a pot experiment. Mycorrhiza 21:403–412

    Article  PubMed  Google Scholar 

  • Koske RE, Gemma JN, Englander L (1990) Vesicular-arbuscular mycorrhizae in Hawaiian Ericales. Am J Bot 77:64–68

    Article  Google Scholar 

  • Kottke I, Haug I, Setaro S, Suárez JP, Weiss M, Preussing M, Nebel M, Oberwinkler F (2008) Guilds of mycorrhizal fungi and their relation to trees, ericads, orchids and liverworts in a neotropical mountain rain forest. Basic Appl Ecol 9:13–23

    Article  CAS  Google Scholar 

  • Kron KA, Luteyn JL (2005) Origins and biogeographic patterns in Ericaceae: new insights from recent phylogenetic analyses. Biol Skr 55:479–500

    Google Scholar 

  • Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of Ericaceae: molecular and morphological evidence. Bot Rev 68:335–423

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Liu G, Chambers SM, Cairney JWG (1998) Molecular diversity of ericoid mycorrhizal endophytes isolated from Woolsia pungens. New Phytol 140:145–153

    Article  CAS  Google Scholar 

  • Lukešová T, Kohout P, Větrovský T, Vohník M (2015) The potential of Dark Septate Endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle European forest plants. PLoS One 10:e0124752

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Massicotte HB, Melville LH, Peterson RL (2005) Structural characteristics of root-fungal interactions for five ericaceous species in eastern Canada. Can J Bot 83:1057–1064

    Article  Google Scholar 

  • McLean C, Lawrie AC (1996) Patterns of root colonization in epacridaceous plants collected from different sites. Ann Bot 77:405–411

    Article  Google Scholar 

  • McLean CB, Cunnington JH, Lawrie AC (1999) Molecular diversity within and between ericoid endophytes from the Ericaceae and Epacridaceae. New Phytol 144:351–358

    Article  CAS  Google Scholar 

  • Midgley DJ, Rosewarne CP, Greenfield P, Li D, Vockler CJ, Hitchcock CJ, Sawyer NA, Brett R, Edwards J, Pitt JI, Tran-Dinh N (2016) Genomic insights into the carbohydrate catabolism of Cairneyella variabilis gen. nov. sp. nov., the first reports from a genome of an ericoid mycorrhizal fungus from the southern hemisphere. Mycorrhiza 26:345–352

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto Y, Sakai A, Hattori M, Nara K (2015) Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains. ISME J 9:1870–1879

    Article  PubMed  PubMed Central  Google Scholar 

  • Molina R, Palmer JG (1982) Isolation, maintenance and pure culture manipulation of ectomycorrhizal fungi. In: Shenk NC (ed) Methods and principles of mycorrhizal research. American Phytopathological Society, Minnesota

    Google Scholar 

  • Monreal M, Berch SM, Berbee M (1999) Molecular diversity of ericoid mycorrhizal fungi. Can J Bot 77:1580–1594

    Article  CAS  Google Scholar 

  • Obase K, Matsuda Y (2014) Culturable fungal endophytes in roots of Enkianthus campanulatus (Ericaceae). Mycorrhiza 24:635–644

    Article  PubMed  Google Scholar 

  • Ohtaka N, Narisawa K (2008) Molecular characterization and endophytic nature of the root-associated fungus Meliniomyces variabilis (LtVB3). J Gen Plant Pathol 74:24–31

    Article  CAS  Google Scholar 

  • Pearson V, Read D (1973a) Biology of mycorrhiza in the Ericaceae II: transport of carbon and phosphorus by endophyte and mycorrhiza. New Phytol 72:1325–1331

    Article  CAS  Google Scholar 

  • Pearson V, Read DJ (1973b) Biology of mycorrhiza in Ericaceae I: isolation of endophyte and synthesis of mycorrhizas in aseptic culture. New Phytol 72:371–379

    Article  Google Scholar 

  • Perotto S, Actis-Perino E, Perugini J, Bonfante P (1996) Molecular diversity of fungi from ericoid mycorrhizal roots. Mol Ecol 5:123–131

    Article  CAS  Google Scholar 

  • Perotto S, Girlanda M, Martino E (2002) Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Plant Soil 244:41–53

    Article  CAS  Google Scholar 

  • Piercey MM, Thormann MN, Currah RS (2002) Saprobic characteristics of three fungal taxa from ericalean roots and their association with the roots of Rhododendron groenlandicum and Picea mariana in culture. Mycorrhiza 12:175–180

    Article  CAS  PubMed  Google Scholar 

  • Põlme S, Bahram M, Yamanaka T, Nara K, Cheng Dai Y, Grebenc T, Kraigher H, Toivonen M, Wang P-H, Matsuda Y, Naadel T, Kennedy PG, Kõljalg U, Tedersoo L (2013) Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol 198:1239–1249

    Article  PubMed  CAS  Google Scholar 

  • Queloz V, Sieber TN, Holdenrieder O, McDonald BA, Grünig CR (2011) No biogeographical pattern for a root-associated fungal species complex. Global Ecol Biogeogr 20:160–169

    Article  Google Scholar 

  • Read DJ (1974) Pezizella ericae sp. nov., the perfect state of a typical mycorrhizal endophyte of Ericaceae. Trans Brit Mycol Soc 63:381–382

    Article  Google Scholar 

  • Read DJ (1983) The biology of mycorrhiza in the Ericales. Can J Bot 61:985–1004

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Reininger V, Sieber TN (2012) Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of conifers. PLoS One 7:e42865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rice AV, Currah RS (2006) Oidiodendron maius: saprobe in Sphagnum peat, mutualist in ericaceous roots? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes, vol 9, Soil Biology Series Vol. Springer, Heidelberg, pp 227–246

    Chapter  Google Scholar 

  • Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Scagel CF (2005) Inoculation with ericoid mycorrhizal fungi alters fertilizer use of highbush blueberry cultivars. HortSci 40:786–794

    Google Scholar 

  • Selosse M-A, Setaro S, Glatard F, Richard F, Urcelay C, Weiss M (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–887

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Vohník M, Chauvet E (2008) Out of the rivers: are some aquatic hyphomycetes plant endophytes? New Phytol 178:3–7

    Article  PubMed  Google Scholar 

  • Setaro SD, Kron K (2011) Neotropical and North American Vaccinioideae (Ericaceae) share their mycorrhizal Sebacinales—an indication for concerted migration? PLOS Currents: Tree of Life. doi:10.1371/currents.RRN1227

    Google Scholar 

  • Setaro S, Weiss M, Oberwinkler F, Kottke I (2006) Sebacinales form ectendomycorrhizas with Cavendishia nobilis, a member of the Andean clade of Ericaceae, in the mountain rain forest of southern Ecuador. New Phytol 169:355–365

    Article  CAS  PubMed  Google Scholar 

  • Sharples JM, Meharg AA, Chambers SM, Cairney JWG (2000a) Mechanism of arsenate resistance in the ericoid mycorrhizal fungus Hymenoscyphus ericae. Plant Physiol 124:1327–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sieber TN (2002) Fungal root endophytes. In: Waisel Y, Eshel A, Kafkafi (eds) Plant roots—the hidden half, 3rd edn. Marcel Dekker, New York

    Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Straker CJ (1996) Ericoid mycorrhiza: ecological and host specificity. Mycorrhiza 6:215–225

    Article  Google Scholar 

  • Straker CJ, Mitchell TD (1985) The characterization and estimation of polyphosphates in endomycorrhizas of the Ericaceae. New Phytol 99:431–440

    Article  CAS  Google Scholar 

  • Stroheker S, Queloz V, Sieber TN (2016) Spatial and temporal dynamics in the Phialocephala fortinii s. l.—Acephala applanata species complex (PAC). Plant Soil. doi:10.1007/s11104-015-2790-0

    Google Scholar 

  • Sun L, Pei K, Wang F, Ding Q, Bing Y, Gao B, Zheng Y, Liang Y, Ma K (2012) Different distribution patterns between putative ericoid mycorrhizal and other fungal assemblages in roots of Rhododendron decorum in the Southwest of China. PLoS One 7:e49867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and other methods), version 4.0 Beta. Sinauer, Sunderland

    Google Scholar 

  • Tian W, Zhang CQ, Qiao P, Milne R (2011) Diversity of culturable ericoid mycorrhizal fungi of Rhododendron decorum in Yunnan, China. Mycologia 103:703–709

    Article  CAS  PubMed  Google Scholar 

  • Toju H, Tanabe AS, Ishii HS (2016) Ericaceous plant–fungus network in a harsh alpine–subalpine environment. Mol Ecol 25:3242–3257

    Article  CAS  PubMed  Google Scholar 

  • Upson R, Read DJ, Newsham KK (2007) Widespread association between the ericoid mycorrhizal fungus Rhizoscyphus ericae and a leafy liverwort in the maritime and sub-Antarctic. New Phytol 176:460–471

    Article  CAS  PubMed  Google Scholar 

  • Urcelay C (2002) Co-occurrence of three fungal root symbionts in Gaultheria poeppiggi DC in Central Argentina. Mycorrhiza 12:89–92

    Article  PubMed  Google Scholar 

  • van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423

    Article  PubMed  CAS  Google Scholar 

  • Villarreal-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

    Article  CAS  Google Scholar 

  • Vohník M, Albrechtová J (2011) The co-occurrence and morphological continuum between ericoid mycorrhiza and dark septate endophytes in roots of six European Rhododendron species. Folia Geobot 46:373–386

    Article  Google Scholar 

  • Vohník M, Albrechtová J, Vosátka M (2005) The inoculation with Oidiodendron maius and Phialocephala fortinii alters phosphorus and nitrogen uptake, foliar C:N ratio and root biomass distribution in Rhododendron cv. Azurro Symbiosis 40:87–96

    Google Scholar 

  • Vohník M, Fendrych M, Albrechtová J, Vosátka M (2007a) 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, Fendrych M, Kolařík M, Gryndler M, Hršelová H, Albrechtová J, Vosátka M (2007b) The ascomycete Meliniomyces variabilis isolated from a sporocarp of Hydnotrya tulasnei (Pezizales) intracellularly colonizes roots of ecto- and ericoid mycorrhizal host plants. Czech Mycol 59:215–226

    Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vohník M, Sadowsky JJ, Lukešová T, Albrechtová J, Vosátka M (2012b) Inoculation with wood decomposing basidiomycete, but not with root symbiotic ascomycetes, positively affects growth of highbush blueberry (Ericaceae) grown in a pine litter substrate. Plant Soil 355:341–352

    Article  CAS  Google Scholar 

  • Vohník M, Mrnka L, Lukešová T, Bruzone MC, Kohout P, Fehrer J (2013) The cultivable endophytic community of Norway spruce ectomycorrhizae from microhabitats lacking ericaceous hosts is dominated by ericoid mycorrhizal Meliniomyces variabilis. Fungal Ecol 6:281–292

    Article  Google Scholar 

  • Vohník M, Pánek M, Fehrer J, Selosse M-A (2016a) Experimental evidence of ericoid mycorrhizal potential within Serendipitaceae (Sebacinales). Mycorrhiza. doi:10.1007/s00572-016-0717-0

    Google Scholar 

  • Vohník M, Borovec O, Kolařík M (2016b) Communities of cultivable root mycobionts of the seagrass Posidonia oceanica in the northwest Mediterranean Sea are dominated by a hitherto undescribed pleosporalean dark septate endophyte. Microb Ecol 71:442–451

    Article  PubMed  Google Scholar 

  • Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza 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 

  • Walker JF, Aldrich-Wolfe L, Riffel A, Barbare H, Simpson NB et al (2011) Diverse Helotiales associated with the roots of three species of Arctic Ericaceae provide no evidence for host specificity. New Phytol 191:515–527

    Article  PubMed  Google Scholar 

  • Wang CJK, Wilcox HE (1985) New species of ectendomycorrhizal and pseudomycorrhizal fungi—Phialophora finlandia, Chloridium paucisporum and Phialocephala fortinii. Mycologia 77:951–958

    Article  Google Scholar 

  • Weiss M, Waller F, Zuccaro A, Selosse M-A (2016) Sebacinales—one thousand and one interactions with land plants. New Phytol 211:20–40

    Article  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis N, Gelfand D, Sninsky J, White T (eds) PCR—protocols and applications—a laboratory manual. Academic, New York

    Google Scholar 

  • Williams AF, Chambers SM, Davies PW, McLean CB, Cairney JWG (2004) Molecular investigation of sterile root-associated fungi from Epacris microphylla R. Br. (Ericaceae) and other epacrids at alpine, subalpine and coastal heathland sites. Australasian Mycologist 23:94–104

    Google Scholar 

  • Wurzburger N, Higgins BP, Hendrick RL (2011) Ericoid mycorrhizal root fungi and their multi-copper oxidases from a temperate forest shrub. Ecol Evol 2:65–79

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zhang C, Yin LJ, Dai SL (2009) Diversity of root-associated fungal endophytes in Rhododendron fortunei in subtropical forests of China. Mycorrhiza 19:417–423

    Article  PubMed  Google Scholar 

  • Zhang Y, Ni J, Tang F, Pei K, Luo Y, Jiang L, Sun L, Liang Y (2016) Root-associated fungi of Vaccinium carlesii in subtropical forests of China: intra- and inter-annual variability and impacts of human disturbances. Sci Rep 6:22399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This study is a part of the long-term research projects of the Institute of Botany CAS (RVO 67985939), Faculty of Science, Charles University in Prague (MŠMT LO1417), and Universidad Nacional del Comahue (04/B143). The authors acknowledge travel stipendiums from the Ministry of Education, Youth and Sports of the Czech Republic (7AMB12AR014 and 7AMB14AR003) and Ministerio de Ciencia, Tecnología e Innovación Productiva de la República Argentina (ARC/11/05 and ARC/13/03). Tereza Lukešová is thanked for the help with isolation of Gaultheria mycobionts, Sebastian Marquez for the help with DNA amplifications, and two anonymous reviewers and Jan Colpaert (editor) for the careful reading of the original manuscript and helpful suggestions for its improvement. MV is grateful to Amaru Magnin for guiding him on the sampling trip and for the interesting conversations in castellano.

Author information

Author notes

    Authors and Affiliations

    1. Laboratorio de Microbiología Aplicada y Biotecnología, Centro Regional Universitario Bariloche, INIBIOMA (Universidad Nacional del Comahue—CONICET), Bariloche, Río Negro, Argentina

      M. Clara Bruzone & Sonia B. Fontenla

    2. DNA Laboratory, Institute of Botany, Czech Academy of Sciences (CAS), Průhonice, CZ-252 43, Czech Republic

      Judith Fehrer

    3. Department of Mycorrhizal Symbioses, Institute of Botany CAS, Průhonice, CZ-252 43, Czech Republic

      Martin Vohník

    4. Department of Plant Experimental Biology, Faculty of Science, Charles University in Prague, Prague, CZ-128 44, Czech Republic

      Martin Vohník

    Authors
    1. M. Clara Bruzone
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Judith Fehrer
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Sonia B. Fontenla
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Martin Vohník
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Martin Vohník.

    Additional information

    M. Clara Bruzone and Judith Fehrer contributed equally to this work.

    Electronic Supplementary Materials

    Below is the link to the electronic supplementary material.

    ESM 1

    Supplementary Table 1 Codes of the isolates obtained in this study. A code starts with “C” when the respective isolate was obtained from Gaultheria caespitosa, with “P” when it was obtained from Gaultheria pumila, and with “B” when it was obtained using the benomyl-amended MMN medium (for details see Materials and Methods). Reference isolates for all OTUs are in bold; their ITS sequences were deposited in GenBank and their accession numbers are listed in Table 1. (PDF 116 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Bruzone, M.C., Fehrer, J., Fontenla, S.B. et al. First record of Rhizoscyphus ericae in Southern Hemisphere’s Ericaceae. Mycorrhiza 27, 147–163 (2017). https://doi.org/10.1007/s00572-016-0738-8

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00572-016-0738-8

    Keywords

    Search

    Navigation