, Volume 27, Issue 5, pp 513–524 | Cite as

Does warming by open-top chambers induce change in the root-associated fungal community of the arctic dwarf shrub Cassiope tetragona (Ericaceae)?

  • Kelsey Erin LorberauEmail author
  • Synnøve Smebye Botnen
  • Sunil Mundra
  • Anders Bjørnsgaard Aas
  • Jelte Rozema
  • Pernille Bronken Eidesen
  • Håvard Kauserud
Original Article


Climate change may alter mycorrhizal communities, which impact ecosystem characteristics such as carbon sequestration processes. These impacts occur at a greater magnitude in Arctic ecosystems, where the climate is warming faster than in lower latitudes. Cassiope tetragona (L.) D. Don is an Arctic plant species in the Ericaceae family with a circumpolar range. C. tetragona has been reported to form ericoid mycorrhizal (ErM) as well as ectomycorrhizal (ECM) symbioses. In this study, the fungal taxa present within roots of C. tetragona plants collected from Svalbard were investigated using DNA metabarcoding. In light of ongoing climate change in the Arctic, the effects of artificial warming by open-top chambers (OTCs) on the fungal root community of C. tetragona were evaluated. We detected only a weak effect of warming by OTCs on the root-associated fungal communities that was masked by the spatial variation between sampling sites. The root fungal community of C. tetragona was dominated by fungal groups in the Basidiomycota traditionally classified as either saprotrophic or ECM symbionts, including the orders Sebacinales and Agaricales and the genera Clavaria, Cortinarius, and Mycena. Only a minor proportion of the operational taxonomic units (OTUs) could be annotated as ErM-forming fungi. This indicates that C. tetragona may be forming mycorrhizal symbioses with typically ECM-forming fungi, although no characteristic ECM root tips were observed. Previous studies have indicated that some saprophytic fungi may also be involved in biotrophic associations, but whether the saprotrophic fungi in the roots of C. tetragona are involved in biotrophic associations remains unclear. The need for more experimental and microscopy-based studies to reveal the nature of the fungal associations in C. tetragona roots is emphasized.


Cassiope tetragona Ericoid mycorrhiza Ectomycorrhiza Svalbard Open-top chambers OTCs Arctic Climate change Root-associated fungi High-throughput sequencing 



The University of Oslo and UNIS are acknowledged for the financial support and for providing lab facilities, while the Research Council of Norway and Svalbard Science Forum are acknowledged for the travel support. Kevin Newsham, David Read, and Ulrik Sochting kindly provided microscopy pictures of Cassiope plant roots.

Supplementary material

572_2017_767_Fig4_ESM.gif (48 kb)
Fig S1

Global nonmetric multidimensional scaling (GNMDS) and detrended correspondence analysis (DCA) ordinations for operational taxonomic unit (OTU) – sample matrices based on (a, b) raw read abundances (c, d) raw read abundances converted to presence/absence, and (e, f) rarefied read abundances converted to presence/absence. The DCA ordinations show clear tongue effects yet confirm the pattern seen in the GNMDS ordinations. Samples from the same location group together and the samples are not separated by warming treatment on either of the first two axes. (GIF 48 kb)

572_2017_767_MOESM1_ESM.eps (15 kb)
High Resolution image (EPS 14 kb)
572_2017_767_Fig5_ESM.png (490 kb)
Fig S2 Micrograph of a Cassiope tetragona hair-root tip taken at 400 x magnification with a Leica DMRB microscope mounted with a Leica DFC420 digital camera. Root sample is unstained, mounted in water, and was collected from Isdammen, Svalbard in August 2014. There is a notable lack of mantle or Hartig net. Micrograph by Kelsey Lorberau. (PNG 489 kb)
572_2017_767_Fig6_ESM.png (540 kb)
Fig S3 Three Cassiope tetragona root micrographs collected from Endalen, Svalbard and stained with trypan blue. Lines indicate ErM hyphal coils. Micrographs courtesy of Kevin Newsham, David Read, and Ulrik Sochting, and taken at 400 x magnification with a Leica DMRB microscope mounted with a Leica DFC420 digital camera. (PNG 539 kb)
572_2017_767_MOESM2_ESM.docx (13 kb)
Table S1 (DOCX 13 kb)
572_2017_767_MOESM3_ESM.docx (15 kb)
Table S2 (DOCX 15 kb)
572_2017_767_MOESM4_ESM.docx (16 kb)
Table S3 (DOCX 15 kb)


  1. Anisimov O, Vaughan D, Callaghan T (2007) Polar regions (Arctic and Antarctic). In: Parry M, Canziani O, Palutikof J et al (eds) Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 653–685Google Scholar
  2. Aronesty E (2013) Comparison of sequencing utility programs. Open Bioinforma J 7:1–8. doi: 10.2174/1875036201307010001 CrossRefGoogle Scholar
  3. Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl Microbiol Biotechnol 87:99–108. doi: 10.1007/s00253-010-2585-4 CrossRefPubMedGoogle Scholar
  4. Bellemain E, Carlsen T, Brochmann C et al (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10:189. doi: 10.1186/1471-2180-10-189 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Birkebak JM, Mayor JR, Ryberg KM, Matheny PB (2013) A systematic, morphological and ecological overview of the Clavariaceae (Agaricales). Mycologia 105:896–911. doi: 10.3852/12-070 CrossRefPubMedGoogle Scholar
  6. Blaalid R, Carlsen T, Kumar S et al (2012) Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol Ecol 21:1897–1908. doi: 10.1111/j.1365-294X.2011.05214.x CrossRefPubMedGoogle Scholar
  7. Blaalid R, Davey ML, Carlsen T et al (2014) Arctic root-associated fungal community composition reflects environmental filtering. Mol Ecol 23:649–659. doi: 10.1111/mec.12622 CrossRefPubMedGoogle Scholar
  8. Blok D, Weijers S, Welker JM et al (2015) Deepened winter snow increases stem growth and alters stem δ 13 C and δ 15 N in evergreen dwarf shrub Cassiope tetragona in high-arctic Svalbard tundra. Environ Res Lett 10:44008. doi: 10.1088/1748-9326/10/4/044008 CrossRefGoogle Scholar
  9. Bokhorst S, Huiskes A, Aerts R et al (2013) Variable temperature effects of open top chambers at polar and alpine sites explained by irradiance and snow depth. Glob Chang Biol 19:64–74. doi: 10.1111/gcb.12028 CrossRefPubMedGoogle Scholar
  10. Botnen S, Vik U, Carlsen T et al (2014) Low host specificity of root-associated fungi at an Arctic site. Mol Ecol 23:975–985. doi: 10.1111/mec.12646 CrossRefPubMedGoogle Scholar
  11. Bougoure DS, Parkin PI, Cairney JWG et al (2007) Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Mol Ecol 16:4624–4636. doi: 10.1111/j.1365-294X.2007.03540.x CrossRefPubMedGoogle Scholar
  12. Buizer B, Weijers S, van Bodegom PM et al (2012) Range shifts and global warming: ecological responses of Empetrum nigrum L. to experimental warming at its northern (high Arctic) and southern (Atlantic) geographical range margin. Environ Res Lett 7:25501. doi: 10.1088/1748-9326/7/2/025501 CrossRefGoogle Scholar
  13. Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740. doi: 10.1046/j.1365-2389.2003.00555.x CrossRefGoogle Scholar
  14. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi: 10.1038/nmeth0510-335 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Clemmensen KE, Michelsen A, Jonasson S, Shaver GR (2006) Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol 171:391–404. doi: 10.1111/j.1469-8137.2006.01778.x CrossRefPubMedGoogle Scholar
  16. 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. doi: 10.1016/j.funeco.2013.02.003 CrossRefGoogle Scholar
  17. Davey M, Blaalid R, Vik U, et al (2015) Primary succession of Bistorta vivipara (L.) Delabre (Polygonaceae) root associated fungi mirrors plant succession in two glacial chronosequences. Environ Microbiol 17:n/a-n/a. doi: 10.1111/1462–2920.12770
  18. Deslippe JR, Hartmann M, Simard SW, Mohn WW (2012) Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol Ecol 82:303–315. doi: 10.1111/j.1574-6941.2012.01350.x CrossRefPubMedGoogle Scholar
  19. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi: 10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  20. Elvebakk A (1994) A survey of the plant associations and alliances from Svalbard. J Veg Sci 5:791–802CrossRefGoogle Scholar
  21. Elvebakk A (1999) Bioclimatic delimitation and subdivision of the Arctic. In: Nordal I, Razzhivin VY (eds) The species concept in the High North—a panarctic flora initiative. Norwegian Academy of Science and Letters, Oslo, pp 81–112Google Scholar
  22. Englander L, Hull RJ (1980) Reciprocal transfer of nutrients between Ericaceous plants and a Clavaria sp. New Phytol 84:661–667CrossRefGoogle Scholar
  23. Feng S, Ho CH, Hu Q et al (2012) Evaluating observed and projected future climate changes for the Arctic using the Köppen-Trewartha climate classification. Clim Dyn 38:1359–1373. doi: 10.1007/s00382-011-1020-6 CrossRefGoogle Scholar
  24. Fujimura KE, Egger KN (2012) Host plant and environment influence community assembly of High Arctic root-associated fungal communities. Fungal Ecol 5:409–418. doi: 10.1016/j.funeco.2011.12.010 CrossRefGoogle Scholar
  25. Fujimura KE, Egger KN, Henry GH (2008) The effect of experimental warming on the root-associated fungal community of Salix arctica. Isme J 2:105–114. doi: 10.1038/ismej.2007.89 CrossRefPubMedGoogle Scholar
  26. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  27. Geml J, Morgado L, Semenova T et al (2015) Long-term warming alters richness and composition of taxonomic and functional groups of Arctic fungi. FEMS Microbiol Ecol 91:1–13CrossRefGoogle Scholar
  28. Grau O, Rautio P, Heikkinen J et al (2010) An ericoid shrub plays a dual role in recruiting both pines and their fungal symbionts along primary succession gradients. Oikos 119:1727–1734. doi: 10.1111/j.1600-0706.2010.18511.x CrossRefGoogle Scholar
  29. Grelet GA, Johnson D, Vralstad T et al (2010) New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytol 188:210–222. doi: 10.1111/j.1469-8137.2010.03560.x CrossRefPubMedGoogle Scholar
  30. Hambleton S, Sigler L (2005) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (=Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27CrossRefGoogle Scholar
  31. Henry GHR, Molau U (1997) Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob Chang Biol 3:1–9. doi: 10.1111/j.1365-2486.1997.gcb132.x CrossRefGoogle Scholar
  32. Hill MO, Gauch HG Jr (1980) Detrended correspondence analysis: an improved ordination technique. Vegetatio 42:47–58CrossRefGoogle Scholar
  33. Hobbie JE, Hobbie EA (2006) 15N in symbiotic fungi and plants estimates nitrogen. Ecology 87:816–822CrossRefPubMedGoogle Scholar
  34. Ihrmark K, Bödeker ITM, Cruz-Martinez K et al (2012) New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677. doi: 10.1111/j.1574-6941.2012.01437.x CrossRefPubMedGoogle Scholar
  35. Katenin A (1964) Mycorrhizae of Arctic plants. Probl Sev 8:148–154Google Scholar
  36. Katenin A (1972) Mycorrhiza in tundra plants of north-east of European part of the USSR. In: Tikhomirov B (ed) The vegetation of the far north of the USSR and its utilization. Botanical Institute Ameni BL Komorova, Leningrad, pp 1–140Google Scholar
  37. Kauserud H, Mathiesen C, Ohlson M (2008) High diversity of fungi associated with living parts of boreal forest bryophytes. Botany 86:1326–1333. doi: 10.1139/B08-102 CrossRefGoogle Scholar
  38. Kohn LM, Stasovski E (1990) The mycorrhizal status of plants at Alexandra Fjord, Ellesmere Island, Canada, a High Arctic site. Mycologia 82:23–35CrossRefGoogle Scholar
  39. Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. doi: 10.1111/mec.12481 CrossRefPubMedGoogle Scholar
  40. Kruskal JB (1964a) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129CrossRefGoogle Scholar
  41. Kruskal JB (1964b) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27. doi: 10.1007/BF02289565 CrossRefGoogle Scholar
  42. Kühdorf K, Münzenberger B, Begerow D et al (2014a) Sebacina sp. is a mycorrhizal partner of Comarostaphylis arbutoides (Ericaceae). Mycol Prog 13:733–744. doi: 10.1007/s11557-013-0956-9 CrossRefGoogle Scholar
  43. Kühdorf K, Münzenberger B, Begerow D, et al (2014b) Leotia cf. lubrica forms arbutoid mycorrhiza with Comarostaphylis arbutoides (Ericaceae). Mycorrhiza 109–120. doi: 10.1007/s00572–014–0590-7
  44. Lindahl BD, Nilsson RH, Tedersoo L et al (2013) Fungal community analysis by high-throughput sequencing of amplified markers—a user’s guide. New Phytol 199:288–299CrossRefPubMedPubMedCentralGoogle Scholar
  45. Liu H-Y, Økland T, Halvorsen R (2008) Gradient analyses of forests ground vegetation and it’s relationship to environmental variables in five subtropical forest areas, S and SW China. Sommerfeltia 32:3–196CrossRefGoogle Scholar
  46. Mallik AU, Wdowiak JV, Cooper EJ (2011) Growth and reproductive responses of Cassiope tetragona, a circumpolar evergreen shrub, to experimentally delayed snowmelt. Arct Antarct Alp Res 43:404–409. doi: 10.1657/1938-4246-43.3.404 CrossRefGoogle Scholar
  47. Marion G, Henry G, Freckman D et al (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3:20–32. doi: 10.1111/j.1365-2486.1997.gcb136.x CrossRefGoogle Scholar
  48. Martos F, Dulormne M, Pailler T et al (2009) Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytol 184:668–681. doi: 10.1111/j.1469-8137.2009.02987.x CrossRefPubMedGoogle Scholar
  49. Michelsen A, Schmidt IK, Jonasson S et al (1996) Leaf N-15 abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63. doi: 10.1007/bf00328791 CrossRefPubMedGoogle Scholar
  50. Miller O Jr (1982) Higher fungi in Alaskan subarctic tundra and taiga plant communities. In: Laursen G, Ammirati J (eds) Arctic and alpine mycology, vol 1. University of Washington Press, Seattle, pp 123–149Google Scholar
  51. Miller O Jr, Laursen G (1974) Belowground fungal biomass on U.S. Tundra Biome sites at Barrow, Alaska. In: Holding A, Heal O, MacLean S, Flanagan P (eds) Soil organisms and decomposition in tundra. Swedish IBP Commitee, Stockholm, pp 151–158Google Scholar
  52. Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107. doi: 10.1007/BF00038690 CrossRefGoogle Scholar
  53. Morgado LN, Semenova TA, Welker JM et al (2015) Summer temperature increase has distinct effects on the ectomycorrhizal fungal communities of moist tussock and dry tundra in Arctic Alaska. Glob Chang Biol 21:959–972. doi: 10.1111/gcb.12716 CrossRefPubMedGoogle Scholar
  54. Mundra S, Bahram M, Tedersoo L et al (2015a) Temporal variation of Bistorta vivipara-associated ectomycorrhizal fungal communities in the High Arctic. Mol Ecol 24:6289–6302. doi: 10.1111/mec.13458
  55. Mundra S, Halvorsen R, Kauserud H, et al (2015b) Arctic fungal communities associated with roots of Bistorta vivipara do not respond to the same fine-scale edaphic gradients as the aboveground vegetation. New Phytol 205:1587–1597Google Scholar
  56. Mundra S, Halvorsen R, Kauserud H et al (2016) Ectomycorrhizal and saprotrophic fungi respond differently to long-term experimentally increased snow depth in the High Arctic. Microbiology 5:856–869. doi: 10.1002/mbo3.375 Google Scholar
  57. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325CrossRefPubMedPubMedCentralGoogle Scholar
  58. Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20CrossRefGoogle Scholar
  59. Nguyen NH, Smith D, Peay K, Kennedy P (2014) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393. doi: 10.1111/nph.12923 CrossRefPubMedGoogle Scholar
  60. Oberwinkler F, Riess K, Bauer R et al (2013) Enigmatic Sebacinales. Mycol Prog 12:1–27. doi: 10.1007/s11557-012-0880-4 CrossRefGoogle Scholar
  61. Oberwinkler F, Riess K, Bauer R, Garnica S (2014) Morphology and molecules: the Sebacinales, a case study. Mycol Prog 13:445–470. doi: 10.1007/s11557-014-0983-1 CrossRefGoogle Scholar
  62. Ogura-Tsujita Y, Gebauer G, Hashimoto T et al (2009) Evidence for novel and specialized mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proc Biol Sci 276:761–767. doi: 10.1098/rspb.2008.1225 CrossRefPubMedGoogle Scholar
  63. Økland RH (1990) Vegetation ecology: theory, methods and applications with reference to Fennoscandia. In: Sommerfeltia Supplementary, 1st edn. pp 1–233Google Scholar
  64. Økland RH (1999) On the variation explained by ordination and constrained ordination axes. J Veg Sci 10:131–136. doi: 10.2307/3237168 CrossRefGoogle Scholar
  65. Økland RH, Eilertsen O (1993) Vegetation-environment relationships of boreal coniferous forests in the Solhomfjell area. Gjerstand, S Norway Sommerfeltia:1–254Google Scholar
  66. Oksanen J, Blanchet FG, Friendly M, et al (2017) vegan: Community Ecology Package.Google Scholar
  67. Park EJ, Lee WY (2013) In vitro symbiotic germination of myco-heterotrophic Gastrodia elata by Mycena species. Plant Biotechnol Rep 7:185–191. doi: 10.1007/s11816-012-0248-x CrossRefGoogle Scholar
  68. Perotto S, Girlanda M, Martino E (2002) Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Plant Soil 244:41–53. doi: 10.1023/A:1020289401610 CrossRefGoogle Scholar
  69. Peters C, Basinger JF, Kaminskyj SGW (2011) Endorhizal fungi associated with vascular plants on Truelove Lowland, Devon Island, Nunavut, Canadian High Arctic. Arctic, Antarct Alp Res 43:73–81CrossRefGoogle Scholar
  70. Peterson JH, Læssøe T (2014) MycoKey 4.1. Accessed January 2016.
  71. Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374. doi: 10.1006/anbo.1996.0044 CrossRefGoogle Scholar
  72. Rønning O (1996) The flora of Svalbard. Norsk PolarinstituttGoogle Scholar
  73. Schadt CW, Rosling A (2015) Comment on “Global diversity and geography of soil fungi”. Science 348:1438–1438. doi: 10.1126/science.aaa426980-CrossRefPubMedGoogle Scholar
  74. Selosse MA, Setaro S, Glatard F et al (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878. doi: 10.1111/j.1469-8137.2007.02064.x CrossRefPubMedGoogle Scholar
  75. Semenchuk PR, Elberling B, Cooper EJ (2013) Snow cover and extreme winter warming events control flower abundance of some, but not all species in High Arctic Svalbard. Ecol Evol 3:2586–2599. doi: 10.1002/ece3.648 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Semenova TA, Morgado LN, Welker JM et al (2015) Long-term experimental warming alters community composition of ascomycetes in Alaskan moist and dry arctic tundra. Mol Ecol 24:424–437. doi: 10.1111/mec.13045 CrossRefPubMedGoogle Scholar
  77. Seviour RJ, Willing RR, Chilvers GA (1973) Basidiocarps associated with ericoid mycorrhizas. New Phytol 72:381–385. doi: 10.1111/j.1469-8137.1973.tb02045.x CrossRefGoogle Scholar
  78. Smith SE, Read D (2008) Mycorrhizal symbiosis, Third edn. Academic PressGoogle Scholar
  79. Strelkova A (1956) Mycorrhizae of plants of tundra and taiga in Taimyr. Bot Zhurnal Leningr 41:1161–1168Google Scholar
  80. Sturm M, Racine C, Tape K (2001) Increasing shrub abundance in the Arctic. Nature 411:546–547. doi: 10.1038/35079180 CrossRefPubMedGoogle Scholar
  81. Stutz R (1972) Survey of mycorrhizal plants. In: Bliss L (ed) Devon Island IPB Project: High Arctic ecosystem. University of Alberta, Edmonton, pp 214–216Google Scholar
  82. Sweet SK, Griffin KL, Steltzer H et al (2015) Greater deciduous shrub abundance extends tundra peak season and increases modeled net CO2 uptake. Glob Chang Biol 21:2394–2409. doi: 10.1111/gcb.12852 CrossRefPubMedGoogle Scholar
  83. Tarnocai C, Canadell JC, Schuur EAG et al (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Glob Biogeochem Cycles 23:1–11. doi: 10.1029/2008GB003327 CrossRefGoogle Scholar
  84. 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. doi: 10.1007/s00572-012-0444-0 CrossRefPubMedGoogle Scholar
  85. Timling I, Walker DA, Nusbaum C et al (2014) Rich and cold: diversity, distribution and drivers of fungal communities in patterned-ground ecosystems of the North American Arctic. Mol Ecol 23:3258–3272CrossRefPubMedGoogle Scholar
  86. Treu R, Laursen GA, Stephenson SL et al (1996) Mycorrhizae from Denali National Park and Preserve, Alaska. Mycorrhiza 6:21–29CrossRefGoogle Scholar
  87. Ugland KI, Gray JS, Ellingsen KE (2003) The species-accumulation curve and estimation of species richness. J Anim Ecol 72:888–897CrossRefGoogle Scholar
  88. Van Son TC, Halvorsen R (2014) Multiple parallel ordinations: the importance of choice of ordination method and weighting of species abundance data. Sommerfeltia 37:1–27. doi: 10.2478/som-2014-0001 CrossRefGoogle Scholar
  89. Villarreal-Ruiz L, Neri-Luna C, Anderson IC, Alexander IJ (2012) In vitro interactions between ectomycorrhizal fungi and ericaceous plants. Symbiosis 56:67–75. doi: 10.1007/s13199-012-0161-7 CrossRefGoogle Scholar
  90. Vohnik M, Panek M, Fehrer J, Selosse M-A (2016) Experimental evidence of ericoid mycorrhizal potential within Serendipitaceae (Sebacinales). Mycorrhiza 26:831–846. doi: 10.1007/s00572-016-0717-0 CrossRefPubMedGoogle Scholar
  91. Vrålstad T (2004) Are ericoid and ectomycorrhizal fungi part of a common guild? New Phytol 164:7–10CrossRefGoogle Scholar
  92. Walker JF, Aldrich-Wolfe L, Riffel A 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. doi: 10.1111/j.1469-8137.2011.03703.x CrossRefPubMedGoogle Scholar
  93. Weiss M, Sykorova Z, Garnica S et al (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS One. doi: 10.1371/journal.pone.0016793 Google Scholar
  94. White TJ, Bruns S, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. pp 315–322Google Scholar
  95. Zhang T, Xiang H-B, Zhang Y-Q et al (2013) Molecular analysis of fungal diversity associated with three bryophyte species in the Fildes Region, King George Island, maritime Antarctica. Extremophiles 17:757–765. doi: 10.1007/s00792-013-0558-0 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Kelsey Erin Lorberau
    • 1
    • 2
    Email author
  • Synnøve Smebye Botnen
    • 1
    • 2
  • Sunil Mundra
    • 1
    • 2
    • 3
  • Anders Bjørnsgaard Aas
    • 1
  • Jelte Rozema
    • 4
  • Pernille Bronken Eidesen
    • 2
  • Håvard Kauserud
    • 1
  1. 1.University of OsloOsloNorway
  2. 2.University Centre in SvalbardLongyearbyenNorway
  3. 3.Biodiversity and Climate Research CentreSenckenberg Gesellschaft für NaturforschungFrankfurt am MainGermany
  4. 4.VU University (Vrije Universiteit) AmsterdamAmsterdamThe Netherlands

Personalised recommendations