Dieback of European Ash: What Can We Learn from the Microbial Community and Species-Specific Traits of Endophytic Fungi Associated with Ash?

  • Ari M. HietalaEmail author
  • Isabella Børja
  • Hugh Cross
  • Nina Elisabeth Nagy
  • Halvor Solheim
  • Volkmar Timmermann
  • Adam Vivian-Smith
Part of the Forestry Sciences book series (FOSC, volume 86)


European ash (Fraxinus excelsior), a keystone species with wide distribution and habitat range in Europe, is threatened at a continental scale by an invasive alien ascomycete, Hymenoscyphus fraxineus. In its native range of Asia, this fungus is a leaf endophyte with weak parasitic capacity and robust saprobic competence in local ash species that are closely related to European ash. In European ash, H. fraxineus has a similar functional role as in Asia, but the fungus also aggressively kills shoots, resulting in crown dieback and tree death. H. fraxineus is a typical invasive species, as its spread relies on high propagule pressure. While crown dieback of European ash is the most obvious symptom of ash dieback, the annual colonization of ash leaves is a crucial key dependency for the invasiveness of H. fraxineus, since its fruiting bodies are formed on overwintered leaf vein tissues in soil debris. Leaves of European ash host a wide range of indigenous epiphytes, endophytes, facultative parasites and biotrophic fungi, including Hymenoscyphus albidus, a relative of H. fraxineus that competes for the same sporulation niche as the invader. At face value, leaves of European ash are colonized by a large and diverse indigenous mycobiome. In order to understand why this invader became successful in Europe, we discuss and summarize the current knowledge of diversity, seasonal dynamics and traits of H. fraxineus and indigenous fungi associated with leaves of European ash.



Next-generation sequencing


Internal transcribed spacer of ribosomal DNA


Quantitative polymerase chain reaction



The writing of this chapter was supported by a strategic institute project focused on forest health and financed by the Norwegian Institute of Bioeconomy Research, the Norwegian Ministry of Agriculture and Food, and the Research Council of Norway. We would like to thank Dr. Anna Maria Pirttilä for valuable comments and careful editing of the manuscript.


  1. Agler MT, Ruhe J, Kroll S et al (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. Scholar
  2. Amselem J, Cuomo CA, van Kan JA et al (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andersson PF, Johansson SBK, Stenlid J et al (2010) Isolation, identification and necrotic activity of viridiol from Chalara fraxinea, the fungus responsible for dieback of ash. For Pathol 40:43–46CrossRefGoogle Scholar
  4. Arnold AE, Mejia LC, Kyllo D et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bakys R, Vasaitis R, Barklund P et al (2009) Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior. Plant Pathol 58:284–292CrossRefGoogle Scholar
  6. Baral HO, Queloz V, Hosoya T (2014) Hymenoscyphus fraxineus, the correct scientific name for the fungus causing ash dieback in Europe. IMA Fungus 5:79PubMedPubMedCentralCrossRefGoogle Scholar
  7. Baral HO, Bemmann M (2014) Hymenoscyphus fraxineus versus Hymenoscyphus albidus – A comparative light microscopic study on the causal agent of European ash dieback and related foliicolous, stroma-forming species. Mycology 5:228–290PubMedPubMedCentralCrossRefGoogle Scholar
  8. Barklund P (2005) Ash dieback takes over south and mid-Sweden. SkogsEko 3:11–13 (In Swedish)Google Scholar
  9. Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339PubMedCrossRefPubMedCentralGoogle Scholar
  10. Burton JN, Liachko I, Dunham MJ, and Shendure J (2014) Species-level deconvolution of metagenome assemblies with Hi-C-based contact probability maps. G3 (Bethesda) 4:1339–1346PubMedPubMedCentralCrossRefGoogle Scholar
  11. Børja I, Solheim H, Nagy NE et al (2017) Hymenoscyphus fraxineus shows population density dependent growth rate. Poster. In: IUFRO 125th Anniversary congress, 18–22 September 2017, Freiburg, GermanyGoogle Scholar
  12. Čermáková V, Kudláček T, Rotková G et al (2017) Hymenoscyphus fraxineus mitovirus 1 naturally disperses through the airborne inoculum of its host, Hymenoscyphus fraxineus, in the Czech Republic. Biocontrol Sci Technol. Scholar
  13. Chandelier A, Helson M, Dvorak M et al (2014) Detection and quantification of airborne inoculum of Hymenoscyphus pseudoalbidus using real-time PCR assays. Plant Pathol 63:1296–1305CrossRefGoogle Scholar
  14. Chen J (2012) Fungal community survey of Fraxinus excelsior in New Zealand. Master thesis, Swedish University of Agricultural Sciences, Uppsala, SwedenGoogle Scholar
  15. Chen L, Yue Q, Zhang X et al (2013) Genomics-driven discovery of the pneumocandin biosynthetic gene cluster in the fungus Glarea lozoyensis. BMC Genom 20:339. Scholar
  16. Chua KH, Lee PC, Chai HC (2016) Development of insulated isothermal PCR for rapid on-site malaria detection. Malaria J 15:134CrossRefGoogle Scholar
  17. Clay K (2004) Fungi and the food of the gods. Nature 427:401–402PubMedCrossRefPubMedCentralGoogle Scholar
  18. Citron C, Junker C, Schulz B et al (2014) A volatile lactone of Hymenoscyphus pseudoalbius, pathogen of ash dieback inhibits host germination. Angew Chem Int Edit 53:4346–4349CrossRefGoogle Scholar
  19. Cleary M, Daniel G, Stenlid J (2013) Light and scanning electron microscopy studies of the early infection stages of Hymenoscyphus pseudoalbidus on Fraxinus excelsior. Plant Pathol 62:1294–1301CrossRefGoogle Scholar
  20. Cleary M, Nguyen D, Marciulyniene D et al (2016) Friend or foe? Biological and ecological traits of the European ash dieback pathogen Hymenoscyphus fraxineus in its native environment. Sci Rep 6:21895PubMedPubMedCentralCrossRefGoogle Scholar
  21. Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 12:157–172Google Scholar
  22. Cordero RJB, Casadevall A (2017) Functions of fungal melanin beyond virulence. Fungal Biol Rev 31:99–112CrossRefGoogle Scholar
  23. Cross H, Sønstebø JH, Nagy NE et al (2017) Fungal diversity and seasonal succession in ash leaves infected by the invasive ascomycete Hymenoscyphus fraxineus. New Phytol 213:1405–1417PubMedCrossRefPubMedCentralGoogle Scholar
  24. Davydenko K, Vasaitis R, Stenlid J et al (2011) Fungi in foliage and shoots of Fraxinus excelsior in eastern Ukraine: a first report on Hymenoscyphus pseudoalbidus. For Pathol 43:462–467CrossRefGoogle Scholar
  25. Dawson W, Moser D, van Kleunen M et al (2017) Global hotspots and correlates of alien species richness across taxonomic groups. Nat Ecol Evol 1:186CrossRefGoogle Scholar
  26. Derbyshire M, Denton-Giles M, Hegedus D et al (2017) The complete genome sequence of the phytopathogenic fungus Sclerotinia sclerotiorum reveals insights into the genome architecture of broad host range pathogens. Genome Biol Evol 9:593–618PubMedCentralCrossRefGoogle Scholar
  27. Develey-Rivière M-P, Galiana E (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol 175:405–416PubMedCrossRefPubMedCentralGoogle Scholar
  28. Drenkhan R, Solheim H, Bogacheva A et al (2017) Hymenoscyphus fraxineus is a leaf pathogen of local Fraxinus species in the Russian Far East. Plant Pathol 66:490–500CrossRefGoogle Scholar
  29. Drayton FL (1932) The sexual function of the microconidia in certain discomycetes. Mycologia 24:345–348CrossRefGoogle Scholar
  30. Dobrowolska D, Hein S, Oosterbaan A et al (2011) A review of European ash (Fraxinus excelsior l.): implications for silviculture. Forestry 84:133–148CrossRefGoogle Scholar
  31. Dvorak M, Rotkova G, Botella L (2016) Detection of airborne inoculum of Hymenoscyphus fraxineus and H. albidus during seasonal fluctuations associated with absence of apothecia. Forests 7(1): 1. Scholar
  32. Engesser R, Queloz V, Meier F et al (2009) Das Triebsterben der Esche in der Schweiz. Wald und Holz 6:24–27Google Scholar
  33. Fauvergue X, Vercken E, Malausa T et al (2012) The biology of small, introduced populations, with special reference to biological control. Evol Appl 5:424–443PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fones HN, Mardon C, Gurr SJ (2016) A role for the asexual spores in infection of Fraxinus excelsior by the ash-dieback fungus Hymenoscyphus fraxineus. Sci Rep 6:34638PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ganley RJ, Brunsfeld SJ, Newcombe G (2004) A community of unknown, endophytic fungi in western white pine. Proc Natl Acad Sci U S A 101:10107–10112PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gianoulis TA, Griffin MA, Spakowicz DJ et al (2012) Genomic analysis of the hydrocarbon-producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet 8:e1002558. Scholar
  38. Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci U S A 104:4979–4983PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gomez BL, Nosanchuk JD (2003) Melanin and fungi. Curr Opin Infect Dis 16:91–96PubMedCrossRefPubMedCentralGoogle Scholar
  40. González-Domínguez E, Armengol J, Rossi V (2017) Biology and Epidemiology of Venturia species affecting fruit crops: a review. Front Plant Sci 8:1496PubMedPubMedCentralCrossRefGoogle Scholar
  41. Grad B, Kowalski T, Kraj W (2009) Studies on secondary metabolite produced by Chalara fraxinea and its phytotoxic influence on Fraxinus excelsior. Phytopathologia 54:61–69Google Scholar
  42. Gross A, Holdenrieder O (2013) On the longevity of Hymenoscyphus pseudoalbidus in petioles of Fraxinus excelsior. For Pathol 43:168–170CrossRefGoogle Scholar
  43. Gross A, Holdenrieder O, Pautasso M et al (2014a) Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. Mol Plant Pathol 15:5–21PubMedCrossRefPubMedCentralGoogle Scholar
  44. Gross A, Hosoya T, Queloz V (2014b) Population structure of the invasive forest pathogen Hymenoscyphus pseudoalbidus. Mol Ecol 23:2943–2960PubMedCrossRefPubMedCentralGoogle Scholar
  45. Gross A, Zaffarano PL, Duo A et al (2012) Reproductive mode and life cycle of the ash dieback pathogen Hymenoscyphus pseudoalbidus. Fungal Genet Biol 49:977–986PubMedCrossRefPubMedCentralGoogle Scholar
  46. Halecker S, Surup F, Kuhnert E et al (2014) Hymenosetin, a 3-decalinoyltetramic acid antibiotic from cultures of the ash dieback pathogen, Hymenoscyphus pseudoalbidus. Phytochemistry 100:86–91PubMedCrossRefPubMedCentralGoogle Scholar
  47. Halecker S, Surup F, Solheim H et al (2017) Albiducins A and B, salicylaldehyde antibiotics from the ash tree-associated saprotrophic fungus Hymenoscyphus albidus. J Antibiot. Scholar
  48. Haňáčková Z, Havrdová L, Černý L et al (2017a) Fungal endophytes in ash shoots – Diversity and inhibition of Hymenoscyphus fraxineus. Balt For 23:89–106Google Scholar
  49. Haňáčková Z, Koukol O, Čmoková A et al (2017b) Direct evidence of Hymenoscyphus fraxineus infection pathway through the petiole-shoot junction. Forest Pathol. Scholar
  50. Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:1293–1320CrossRefGoogle Scholar
  51. Hietala AM, Timmermann V, Børja I et al (2013) The invasive ash dieback pathogen Hymenoscyphus pseudoalbidus exerts maximal infection pressure prior to the onset of host leaf senescence. Fungal Ecol 6:302–308CrossRefGoogle Scholar
  52. Heil CS, Burton JN, Liachko I, et al (2017) Identification of a novel interspecific hybrid yeast from a metagenomic spontaneously inoculated beer sample using Hi-C. Yeast.
  53. Henriksen S, Hilmo O (eds) (2015) Norsk rødliste for arter 2015 [Norwegian red list for species 2015]. Artsdatabanken, Norway (in Norwegian)Google Scholar
  54. Hosoya T, Otani Y, Furuya K (1993) Materials for the fungus flora of Japan (46). Trans Mycol Soc Jpn 34:429–432Google Scholar
  55. Ibrahim M, Schlegel M, Sieber TN (2016) Venturia orni sp. nov, a species distinct from Venturia fraxini, living in the leaves of Fraxinus ornus. Mycol Prog 15:29Google Scholar
  56. Jumpponen A, Jones K (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513PubMedCrossRefPubMedCentralGoogle Scholar
  57. Junker C (2013) Pathogenese und Ansätze zur Kontrolle von Hymenoscyphus pseudoalbidus – Erreger des Eschentriebsterbens: Variabilität von Virulenz, Morphologie, Biochemie und Sekundärstoffwechsel. Ph.D. thesis, Braunschweig University of Technology, GermanyGoogle Scholar
  58. Junker C, Mandey F, Pais A et al (2014) Hymenoscyphus pseudoalbidus and Hymenoscyphus albidus: viridiol concentration and virulence do not correlate. For Pathol 44:39–44CrossRefGoogle Scholar
  59. Kennedy TA, Naeem S, Howe KM et al (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638PubMedCrossRefPubMedCentralGoogle Scholar
  60. Kimura N, Tsuge T (1993) Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol 175:4427–4435PubMedPubMedCentralCrossRefGoogle Scholar
  61. King KM, Webber JF (2016) Development of a multiplex PCR assay to discriminate native Hymenoscyphus albidus and introduced Hymenoscyphus fraxineus in Britain and assess their distribution. Fungal Ecol 23:79–85CrossRefGoogle Scholar
  62. Kirisits T (2015) Ascocarp formation of Hymenoscyphus fraxineus on several-year-old pseudosclerotial leaf rachises of Fraxinus excelsior. For Pathol 45:254–257CrossRefGoogle Scholar
  63. Kirisits T, Matlakova M, Mottinger-Kroupa S et al (2009) The current situation of ash dieback caused by Chalara fraxinea in Austria. In: Doğmuş-Lehtijärvi T (ed) Proceedings of the IUFRO working party 7.02.02. Eğirdir, Turkey, 11–16 May 2009, p 21. Isparta, Turkey: Süleyman Demirel University, Faculty of ForestryGoogle Scholar
  64. Koukol O, Haňáčková Z, Dvořák M et al (2016) Unseen, but still present in Czechia: Hymenoscyphus albidus detected by real-time PCR, but not by intensive sampling. Mycol Prog 15:1–9CrossRefGoogle Scholar
  65. Kowalski T (2006) Chalara fraxinea sp.nov. associated with dieback of ash (Fraxinus excelsior) in Poland. For Pathol 36:264–270CrossRefGoogle Scholar
  66. Kowalski T, Bartnik C (2010) Morphological variation in colonies of Chalara fraxinea isolated from ash (Fraxinus excelsior L.) stems with symptoms of dieback and effects of temperature on colony growth and structure. Acta Agrobot 63:99–106CrossRefGoogle Scholar
  67. Kowalski T, Holdenrieder O (2009) The teleomorph of Chalara fraxinea, the causal agent of ash dieback. For Pathol 39:304–308CrossRefGoogle Scholar
  68. Kowalski T, Bialobrzeski M, Ostafinska A (2013) The occurrence of Hymenoscyphus pseudoalbidus apothecia in the leaf litter of Fraxinus excelsior stands with ash dieback symptoms in southern Poland. Acta Mycol 48:135–146CrossRefGoogle Scholar
  69. Kuemmerle T, Levers C, Erb K et al (2016) Hotspots of land use change in Europe. Environ Res Lett 11: Article 064020CrossRefGoogle Scholar
  70. Kuske CR, Hesse CN, Challacombe F (2015) Prospects and challenges for fungal metatranscriptomics of complex communities. Fungal Ecol 14:133–137CrossRefGoogle Scholar
  71. Laforest-Lapointe I, Paguette A, Messier C et al (2017) Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546:145–147PubMedPubMedCentralCrossRefGoogle Scholar
  72. Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26CrossRefGoogle Scholar
  73. Liao HL, Chen Y, Bruns TD et al (2014) Metatranscriptomic analysis of ectomycorrhizal roots reveals genes associated with Piloderma-Pinus symbiosis: improved methodologies for assessing gene expression in situ. Environ Microbiol 16:3730–3742PubMedCrossRefPubMedCentralGoogle Scholar
  74. Maheshwari R (1999) Microconidia of Neurospora crassa. Fungal Genet Biol 26:1–18PubMedCrossRefPubMedCentralGoogle Scholar
  75. Manoharan L, Kushwaha SK, Hedlund K et al (2015) Captured metagenomics: large-scale targeting of genes based on ‘sequence capture’ reveals functional diversity in soils. DNA Res 22:451–460PubMedPubMedCentralCrossRefGoogle Scholar
  76. Marigo G, Peltier JP, Girel J et al (2000) Success in the demographic expansion of Fraxinus excelsior L. Trees 15:1–13CrossRefGoogle Scholar
  77. McKinney LV, Nielsen LR, Collinge DB et al (2014) The ash dieback crisis: genetic variation in resistance can prove a long-term solution. Plant Pathol 63:485–499CrossRefGoogle Scholar
  78. McKinney LV, Thomsen IM, Kjaer ED et al (2012) Rapid invasion by an aggressive pathogenic fungus (Hymenoscyphus pseudoalbidus) replaces a native decomposer (Hymenoscyphus albidus): a case of local cryptic extinction? Fungal Ecol 5:663–669CrossRefGoogle Scholar
  79. McMullan M, Rafiqi M, Kaithakottil G et al (2017) The ash dieback invasion of Europe was founded by two individuals from a native population with huge adaptive potential. BioRxiv
  80. Minenko E, Vogel RF, Niessen L (2014) Application of one-step reverse transcription loop mediated isothermal amplification (reverse transcripton LAMP) for rapid detection of fungal gene expression in pure culture mycelia and in planta. Mycoscience 55:425–430CrossRefGoogle Scholar
  81. Morf J, Wingett SW, Farabella I et al (2017) Spatial RNA proximities reveal a bipartite nuclear transcriptome and territories of differential density and transcription elongation rates. BioRxiv
  82. Nielsen LR, McKinney LV, Hietala AM et al (2017) The susceptibility of Asian, European and North American Fraxinus species to the ash dieback pathogen Hymenoscyphus fraxineus reflects their phylogenetic history. Eur J For Res 136:59–73CrossRefGoogle Scholar
  83. Paini DR, Sheppard AW, Cook DC et al (2016) Global threat to agriculture from invasive species. Proc Natl Acad Sci U S A 113:7575–7579PubMedPubMedCentralCrossRefGoogle Scholar
  84. Pautasso M, Aas G, Queloz V et al (2013) European ash (Fraxinus excelsior) dieback – A conservation biology challenge. Biol Conserv 158:37–49CrossRefGoogle Scholar
  85. Petrini L, Petrini O (1985) Xylariaceous fungi as endophytes. Sydowia. Ann Mycol Ser II 38:216–234Google Scholar
  86. Plissonneau C, Benevenuto J, Mohd-Assaad N et al (2017) Using population and comparative genomics to understand the genetic basis of effector-driven fungal pathogen evolution. Front Plant Sci 8:1–15CrossRefGoogle Scholar
  87. Pomerantz A, Penafiel N, Arteaga A et al (2017) Real-time DNA barcoding in a remote rainforest using nanopore sequencing. BioRiv
  88. Poudel R, Jumpponen A, Schlatter DC et al (2016) Microbiome Networks: a systems framework for identifying candidate microbial assemblages for disease management. Phytopathology 106:1083–1096PubMedCrossRefPubMedCentralGoogle Scholar
  89. Press MO, Wiser AH, Kronenberg ZN et al (2017) Hi-C deconvolution of a human gut microbiome yields high-quality draft genomes and reveals plasmid-genome interactions. BioRxiv
  90. Pliūra A, Bakys R, Suchockas V et al (2017) Ash dieback in Lithuania: disease history, research on impact and genetic variation in disease resistance, tree breeding and options for forest management. In: Vasaitis R, Enderle R (eds) Dieback of European ash (Fraxinus spp.): consequences and guidelines for sustainable management. Swedish University of Agricultural Sciences, pp 150–165. ISBN (print version) 978-91-576-8696-1, ISBN (electronic version) 978-91-576-8697-8Google Scholar
  91. Przybył K (2002) Fungi associated with necrotic apical parts of Fraxinus excelsior shoots. For Pathol 32:387–394CrossRefGoogle Scholar
  92. Queloz V, Grunig CR, Berndt R et al (2011) Cryptic speciation in Hymenoscyphus albidus. For Pathol 41:133–142CrossRefGoogle Scholar
  93. Reiher DBA (2011) Leaf-inhabiting endophytic fungi in the canopy of the Leipzig floodplain forest. Ph.D. thesis, University of Leipzig, Leipzig, GermanyGoogle Scholar
  94. Rodriguez RJ, White JF Jr, Arnold AE et al (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sambles C, Moore K, Kershaw M et al (2015) Genome sequencing of nine species from the genus, Hymenoscyphus. Accessed 16 Oct 2017
  96. Schlegel M, Dubach V, von Buol L et al (2016) Effects of endophytic fungi on the ash dieback pathogen. FEMS Microbiol Ecol 92.
  97. Schoebel CN, Botella L, Lygis V et al (2017) Population genetic analysis of a parasitic mycovirus to infer the invasion history of its fungal host. Mol Ecol. Scholar
  98. Scholtysik A, Unterseher M, Otto P et al (2013) Spatio-temporal dynamics of endophyte diversity in the canopy of European ash (Fraxinus excelsior). Mycol Prog 12:291–304CrossRefGoogle Scholar
  99. Schubert K, Ritschel A, Braun U (2003) A monograph of Fusicladium (Hyphomycetes). Schlechtendalia 9:1–132Google Scholar
  100. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedPubMedCentralCrossRefGoogle Scholar
  101. Schulz B, Boyle C, Draeger S et al (2002) Endophytic fungi: a source of biologically active secondary metabolites. Mycol Res 106:996–1004CrossRefGoogle Scholar
  102. Schulz B, Haas S, Junker C et al (2015) Fungal endophytes involved in multiple balanced antagonisms. Curr Sci 109:39–45Google Scholar
  103. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89CrossRefGoogle Scholar
  104. Simberloff D (2009) The role of propagule pressure in biological invasions. Ann Rev Ecol Evol S 40:81–102CrossRefGoogle Scholar
  105. Solheim H, Hietala AM (2017) Spread of ash dieback in Norway. Balt For 23:144–149Google Scholar
  106. Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates Inc., Massachusetts, pp 41–64Google Scholar
  107. Steinböck S (2013) Ash dieback caused by Hymenoscyphus pseudoalbidus in Norway: phenology and etiology of leaf symptoms and ascospore dispersal distances. Master thesis, University of Natural Resources and Life Sciences, Vienna, AustriaGoogle Scholar
  108. Stenlid J, Elfstrand M, Cleary M et al (2017) Genomes of Hymenoscyphus fraxineus and Hymenoscyphus albidus encode surprisingly large cell wall degrading potential, balancing saprotrophic and necrotrophic signatures. Balt For 23:41–51Google Scholar
  109. Suenaga H (2012) Targeted metagenomics: a high-resolution metagenomics approach for specific gene clusters in complex microbial communities. Environ Microbiol 14:13–22PubMedCrossRefPubMedCentralGoogle Scholar
  110. Sønstebø JH, Vivian-Smith A, Adamson K et al (2017) Genome-wide population diversity in Hymenoscyphus fraxineus points to an eastern Russian origin of European Ash dieback. BioRxiv. Scholar
  111. Talgø V, Sletten A, Brurberg MB et al (2009) Chalara fraxinea isolated from diseased ash in Norway. Plant Dis 95:548CrossRefGoogle Scholar
  112. Tilman D (2004) A stochastic theory of resource competition, community assembly and invasions. Proc Natl Acad Sci U S A 101:10854–10861PubMedPubMedCentralCrossRefGoogle Scholar
  113. Timmermann V, Børja I, Hietala AM et al (2011) Ash dieback: pathogen spread and diurnal patterns of ascospore dispersal, with special emphasis on Norway. EPPO Bull 41:14–20CrossRefGoogle Scholar
  114. Timmermann V, Nagy NE, Hietala AM et al (2017) Progression of ash dieback in Norway related to tree age, disease history and regional aspects. Balt For 23:150–158Google Scholar
  115. Trapiello E, Schoebel CN, Rigling D (2017) Fungal community in symptomatic ash leaves in Spain. Balt For 23:68–73Google Scholar
  116. Truong C, Mujic AB, Healy R et al (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214:913–919PubMedCrossRefPubMedCentralGoogle Scholar
  117. Unterseher M, Reiher A, Finstermeier K et al (2007) Species richness and distribution patterns of leaf-inhabiting endophytic fungi in a temperate forest canopy. Mycol Prog 6:201–212CrossRefGoogle Scholar
  118. Vasaitis R, Enderle R (eds) (2017) Dieback of European Ash (Fraxinus spp.) – Consequences and guidelines for sustainable management. Swedish University of Agricultural Sciences, 320 p. ISBN (print version) 978-91-576-8696-1, ISBN (electronic version) 978-91-576-8697-8Google Scholar
  119. Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytol 159:93–100CrossRefGoogle Scholar
  120. Voříšková J, Baldrian P (2013) Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME J 7:477–486PubMedCrossRefPubMedCentralGoogle Scholar
  121. van der Heijden MGA, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol. Scholar
  122. van Kan JAL, Stassen JHM, Mosbach A et al (2017) A gapless genome sequence of the fungus Botrytis cinerea. Mol Plant Pathol 18:75–89PubMedCrossRefPubMedCentralGoogle Scholar
  123. Wallander E (2008) Systematics of Fraxinus (Oleaceae) and evolution of dioecy. Plant Syst Evol 273:25–49CrossRefGoogle Scholar
  124. Wang Z, Johnston PR, Yang ZL et al (2009) Evolution of reproductive morphology in leaf endophytes. PLoS ONE 4(1):e4246PubMedPubMedCentralCrossRefGoogle Scholar
  125. Youssara L, Grüning BA, Erxleben A (2012) Genome sequence of the fungus Glarea lozoyensis: the first genome sequence of a species from the Helotiaceae family. Eukaryot Cell 11:250CrossRefGoogle Scholar
  126. Zhao YJ, Hosoya T, Baral H-O et al (2013) Hymenoscyphus pseudoalbidus, the correct name for Lambertella albida reported from Japan. Mycotaxon 122:25–41CrossRefGoogle Scholar
  127. Zheng HD, Zhuang WY (2014) Hymenoscyphus albidoides sp. nov. and H. pseudoalbidus from China. Mycol Prog 13:625–638CrossRefGoogle Scholar
  128. Zhu S, Cao YZ, Jiang C (2012) Sequencing the genome of Marssonina brunnea reveals fungus-poplar co-evolution. BMC Genom 9:382CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ari M. Hietala
    • 1
    Email author
  • Isabella Børja
    • 1
  • Hugh Cross
    • 2
  • Nina Elisabeth Nagy
    • 1
  • Halvor Solheim
    • 1
  • Volkmar Timmermann
    • 1
  • Adam Vivian-Smith
    • 1
  1. 1.Norwegian Institute of Bioeconomy ResearchÅsNorway
  2. 2.Department of AnatomyUniversity of OtagoDunedinNew Zealand

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