Toxigenic Foliar Endophytes from the Acadian Forest

  • Joey B. Tanney
  • David R. McMullin
  • J. David Miller
Part of the Forestry Sciences book series (FOSC, volume 86)


This chapter describes the ecology of foliar endophytes of the Acadian Forest that dominates Canada’s Maritime Provinces extending into Eastern Quebec and Maine. Recent evidence has illuminated the ‘foraging ascomycete’ life habit of fungi that can be endophytic in conifer needles. These fungi can occupy several eco-niches other than the needles including as saprophytes in aquatic or terrestrial environments or as endophytes of understory species. Structurally diverse secondary antifungal and antiinsectan metabolites appear to mediate the exchange between plant and fungus. The plant provides nutrients and shelter, the fungus increases plant fitness by contributing to tolerance to herbivorous insects or needle pathogens. This work is enabled by the advent of affordable sequencing capability, a dedication to fieldwork and alpha taxonomy, and directed investigations of the metabolites produced by these interesting fungi.



We thank many undergraduate and graduate students and post-doctoral fellows who have contributed to this research over the past three decades. We are grateful for the support and advice of Greg Adams, Shona Millican and Andrew McCartney from JD Irving Limited, Dr. Keith Seifert from Agriculture Agi-Food Canada (Ottawa), and Prof. David Malloch. We thank the Natural Sciences and Engineering Research Council of Canada, the Province of Ontario through the Mitacs program and JD Irving Limited for supporting this research. Jason Karakehian kindly provided the image of Colpoma crispum (Fig. 9d).


  1. Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T (2010) The UNITE database for molecular identification of fungi–recent updates and future perspectives. New Phytol 186:281–285PubMedPubMedCentralGoogle Scholar
  2. Allen E, Humble L (2002) Nonindigenous species introductions: a threat to Canada’s forests and forest economy. Can J Plant Path 24:103–110CrossRefGoogle Scholar
  3. Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16CrossRefGoogle Scholar
  4. Amos-Binks LJ, MacLean DA et al (2010) Temporal changes in species composition of mixed wood stands in northwest New Brunswick: 1946–2008. Can J For Res 40:1–12CrossRefGoogle Scholar
  5. Ando K (1992) A study of terrestrial aquatic hyphomycetes. Trans Mycol Soc Jpn 33:415–425Google Scholar
  6. Anke H, Stadler M, Mayer A, Sterner O (1995) Secondary metabolites with nematicidal and antimicrobial activity from nematophagous fungi and Ascomycetes. Can J Bot 73:932–939CrossRefGoogle Scholar
  7. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549PubMedPubMedCentralCrossRefGoogle Scholar
  8. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci 100:15649–15654PubMedPubMedCentralCrossRefGoogle Scholar
  9. Badotti F, de Oliveira FS, Garcia CF, Vaz ABM, Fonseca PLC, Nahum LA, Oliveira G, Góes-Neto A (2017) Effectiveness of ITS and sub-regions as DNA barcode markers for the identification of Basidiomycota (Fungi). BMC Microbiol 17:42PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bandoni RJ, Koske RE (1974) Monolayers and microbial dispersal. Science 183:1079–1081PubMedCrossRefGoogle Scholar
  11. Barengo N, Sieber TN, Holdenrieder O (2000) Diversity of endophytic mycobiota in leaves and twigs of pubescent birch (Betula pubescens). Sydowia 52:305–320Google Scholar
  12. Barklund P (1987) Occurrence and pathogenicity of Lophodermium piceae appearing as an endophyte in needles of Picea abies. Trans Br Mycol Soc 89:307–313CrossRefGoogle Scholar
  13. Barklund P, Kowalski T (1996) Endophytic fungi in branches of Norway spruce with particular reference to Tryblidiopsis pinastri. Can J Bot 74:673–678CrossRefGoogle Scholar
  14. Bills GF, González-Menéndez V, Martín J, Platas G, Fournier J, Peršoh D, Stadler M (2012) Hypoxylon pulicicidum sp. nov. (Ascomycota, Xylariales), a pantropical insecticide-producing endophyte. PLoS ONE 7:e46687PubMedPubMedCentralCrossRefGoogle Scholar
  15. Blais J (1983) Trends in the frequency, extent, and severity of spruce budworm outbreaks in eastern Canada. Can J For Res 13:539–547CrossRefGoogle Scholar
  16. Botella L, Diez JJ (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18CrossRefGoogle Scholar
  17. Broders K, Munck I, Wyka S, Iriarte G, Beaudoin E (2015) Characterization of fungal pathogens associated with white pine needle damage (WPND) in Northeastern North America. Forests 6:4088–4104CrossRefGoogle Scholar
  18. Butin VH, Kowalski T (1990) Die natürliche Astreinigung und ihre biologischen Voraussetzungen V. Die Pilzflor.von Fichte, Kiefer und Lärche. Eur J For Pathol 20:44–54CrossRefGoogle Scholar
  19. Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286CrossRefGoogle Scholar
  20. Carroll GC (1999) The foraging ascomycete. In: 16th International Botanical Congress, St. Louis, MO, USAGoogle Scholar
  21. Chang W-Y, Lantz VA, Hennigar CR, MacLean DA (2012) Economic impacts of forest pests: a case study of spruce budworm outbreaks and control in New Brunswick, Canada. Can J For Res 42:490–505CrossRefGoogle Scholar
  22. Chauvet E, Cornut J, Sridhar KR, Selosse M-A, Bärlocher F (2016) Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecol 19:112–127CrossRefGoogle Scholar
  23. Chaverri P, Gazis RO (2011) Linking ex planta fungi with their endophytic stages: Perisporiopsis, a common leaf litter and soil fungus, is a frequent endophyte of Hevea spp. and other plants. Fungal Ecol 4:94–102CrossRefGoogle Scholar
  24. Chen C, Verkley GJ, Sun G, Groenewald JZ, Crous PW (2015) Redefining common endophytes and plant pathogens in Neofabraea, Pezicula, and related genera. Fungal Biol 120:1291–1322PubMedCrossRefGoogle Scholar
  25. Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16CrossRefGoogle Scholar
  26. Claydon N, Grove JF, Pople M (1985) Elm bark beetle boring and feeding deterrents from Phomopsis oblonga. Phytochemistry 24:937–943CrossRefGoogle Scholar
  27. Czabator F, Staley J, Snow G (1971) Extensive southern pine needle blight during 1970–1971, and associated fungi. Plant Dis Rep 55:764–766Google Scholar
  28. Darker GD (1967) A revision of the genera of the Hypodermataceae. Can J Bot 45:1399–1444CrossRefGoogle Scholar
  29. Davis EC, Franklin JB, Shaw AJ, Vilgalys R (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 90:1661–1667PubMedCrossRefPubMedCentralGoogle Scholar
  30. de Beer Z, Marincowitz S, Duong T, Kim J, Rodrigues A, Wingfield M (2016) Hawksworthiomyces gen. nov. (Ophiostomatales) Hawksworthiomyces gen. nov. (Ophiostomatales), illustrates the urgency for a decision on how to name novel taxa known only from environmental nucleic acid sequences (ENAS). Fungal Biol 120:1323–1340PubMedCrossRefPubMedCentralGoogle Scholar
  31. Deckert RJ, Melville LH, Peterson RL (2001) Structural features of a Lophodermium endophyte during the cryptic life-cycle phase in the foliage of Pinus strobus. Mycol Res 105:991–997CrossRefGoogle Scholar
  32. Dreyfuss M, Petrini O (1984) Further investigations on the occurrence and distribution of endophytic fungi in tropical plants. Bot Helv 94:33–40Google Scholar
  33. Dymond CC, Neilson ET, Stinson G, Porter K, MacLean DA, Gray DR, Campagna M, Kurz WA (2010) Future spruce budworm outbreak may create a carbon source in eastern Canadian forests. Ecosystems 13:917–931CrossRefGoogle Scholar
  34. Etheridge DA, MacLean DA, Wagner RG et al (2005) Changes in landscape composition and stand structure from 1945–2002 on an industrial forest in New Brunswick, Canada. Can J For Res 35:1965–1977CrossRefGoogle Scholar
  35. Etheridge DA, MacLean DA, Wagner RG, Wilson JS (2006) Effects of intensive forest management on stand and landscape characteristics in northern New Brunswick, Canada (1945–2027). Landscape Ecol 21:509–524CrossRefGoogle Scholar
  36. Et-Touil K, Bernier L, Beaulieu J, Bérubé J, Hopkin A, Hamelin R (1999) Genetic structure of Cronartium ribicola populations in eastern Canada. Phytopathology 89:915–919PubMedCrossRefGoogle Scholar
  37. Farr D, Rossman A (2016). Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved 25 Sept 2017, from
  38. Findlay JA, Buthelezi S, Lavoie R, Peña-Rodriguez L, Miller JD (1995) Bioactive isocoumarins and related metabolites from conifer endophytes. J Nat Prod 58:1759–1766PubMedCrossRefGoogle Scholar
  39. Findlay JA, Li G, Miller JD, Womiloju TO (2003) Insect toxins from spruce endophytes. Can J Chem 81:284–292CrossRefGoogle Scholar
  40. Fleming RA, Candau J-N, McAlpine RS (2002) Landscape-scale analysis of interactions between insect defoliation and forest fire in central Canada. Clim Change 55:251–272CrossRefGoogle Scholar
  41. Frasz SL, Walker AK, Nsiama TK, Adams GW, Miller JD (2014) Distribution of the foliar fungal endophyte Phialocephala scopiformis and its toxin in the crown of a mature white spruce tree as revealed by chemical and qPCR analyses. Can J For Res 44:1138–1143CrossRefGoogle Scholar
  42. Gao Y, Liu F, Cai L (2016) Unravelling Diaporthe species associated with Camellia. Syst Biodivers 14:102–117CrossRefGoogle Scholar
  43. Gazis R, Rehner S, Chaverri P (2011) Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol 20:3001–3013PubMedCrossRefPubMedCentralGoogle Scholar
  44. Gönczöl J, Révay Á (2004) Fungal spores in rainwater: stemflow, throughfall and gutter conidial assemblages. Fungal Divers 16:67–86Google Scholar
  45. Green BD (2016). Characterization of secondary metabolites produced by foliar endophytes of red and black spruce. MSc. Thesis. Department of Chemistry, Carleton University OttawaGoogle Scholar
  46. Greenfield M, Pareja R, Ortiz V, Gómez-Jiménez MI, Vega FE, Parsa S (2015) A novel method to scale up fungal endophyte isolations. Biocontrol Sci Technol 25:1208–1212CrossRefGoogle Scholar
  47. Grove JF (1985) Metabolic products of Phomopsis oblonga. Part 2. Phomopsolide A and B, tiglic esters of two 6-substituted 5, 6-dihydro-5-hydroxypyran-2-ones. J Chem Soc, Perkin Trans 1:865–869CrossRefGoogle Scholar
  48. Grünig CR, Queloz V, Duò A, Sieber TN (2009) Phylogeny of Phaeomollisia piceae gen. sp. nov.: a dark, septate, conifer-needle endophyte and its relationships to Phialocephala and Acephala. Mycol Res 113:207–221PubMedCrossRefPubMedCentralGoogle Scholar
  49. Haemmerli UA, Brändle UE, Petrini O, McDermott JM (1992) Differentiation of isolates of Discula umbrinella (Teleomorph: Apiognomonia errabunda) from beech, chestnut, and oak using randomly amplified polymorphic DNA markers. MPMI 5:479–483PubMedCrossRefPubMedCentralGoogle Scholar
  50. Hanada RE, Pomella AWV, Costa HS, Bezerra JL, Loguercio LL, Pereira JO (2010) Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuaçu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol 114:901–910PubMedCrossRefPubMedCentralGoogle Scholar
  51. Hawksworth DL, Hibbett DS, Kirk PM, Lücking R (2016) (308–310) Proposals to permit DNA sequence data to serve as types of names of fungi. Taxon 65:899–900CrossRefGoogle Scholar
  52. Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11:129–133PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hibbett D, Abarenkov K, Kõljalg U, Öpik M, Chai B, Cole J, Wang Q, Crous P, Robert V, Helgason T (2016) Sequence-based classification and identification of Fungi. Mycologia 108:1049–1068PubMedPubMedCentralGoogle Scholar
  54. Hom J, Oechel W (1983) The photosynthetic capacity, nutrient content, and nutrient use efficiency of different needle age-classes of black spruce (Picea mariana) found in interior Alaska. Can J For Res 13:834–839CrossRefGoogle Scholar
  55. Horn WS, Simmonds MS, Schwartz RE, Blaney WM (1996) Variation in production of phomodiol and phomopsolide B by Phomopsis spp. Mycologia: 588–595Google Scholar
  56. Huang Y-L, Devan MN, U’Ren JM, Furr SH, Arnold AE (2016) Pervasive effects of wildfire on foliar endophyte communities in montane forest trees. Microb Ecol 71:452–468PubMedCrossRefPubMedCentralGoogle Scholar
  57. Ibrahim A, Fei F, Tanney JB, McDowell T, Ejim L, Seifert KA, Sørensen D, Capretta A, Sumarah MW (2018) Metabome-guided discovery of cyclic non-ribosomal peptides from Xylaria elissi—a new griseofulvin-producing endophyte from Vaccinium angustifolium (in preparation)Google Scholar
  58. Isaka M, Tanticharoen M, Thebtaranonth Y (2000) Cordyanhydrides A and B. Two unique anhydrides from the insect pathogenic fungus Cordyceps pseudomilitaris BCC 1620. Tetrahedron Lett 41:1657–1660CrossRefGoogle Scholar
  59. Jalkanen R, Laakso R (1986) Hendersonia acicola in an epidemic caused by Lophodermella sulcigena with special reference to biological control. Karstenia 26:49–56CrossRefGoogle Scholar
  60. Johnson JA, Whitney NJ (1989) An investigation of needle endophyte colonization patterns with respect to height and compass direction in a single crown of balsam fir (Abies balsamea). Can J Botany 67:723–725CrossRefGoogle Scholar
  61. Jumpponen A, Jones K (2009) Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 184:438–448PubMedCrossRefGoogle Scholar
  62. Kehr R (1992) Pezicula canker of Quercus rubra L., caused by Pezicula cinnamomea (DC.) Sacc. II. Morphology and biology of the causal agent. For Pathol 22:29–40CrossRefGoogle Scholar
  63. Khan Z, Rho H, Firrincieli A, Hung SH, Luna V, Masciarelli O, Kim S-H, Doty SL (2016) Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Curr Plant Biol 6:38–47CrossRefGoogle Scholar
  64. Kirk P, Cannon P, Minter D, Stalpers J (2008) Dictionary of the Fungi, 10th edn. CAB International, University Press, CambridgeGoogle Scholar
  65. Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous P (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35:87–100CrossRefGoogle Scholar
  66. Koukol O, Kolařík M, Kolářová Z, Baldrian P (2012) Diversity of foliar endophytes in wind-fallen Picea abies trees. Fungal Divers 54:69–77CrossRefGoogle Scholar
  67. Kowalski T, Kehr R (1992) Endophytic fungal colonization of branch bases in several forest tree species. Sydowia 44:137–168Google Scholar
  68. Kowalski T, Kehr R (1995) Two new species of Phialocephala occurring on Picea and Alnus. Can J Bot 73:26–32CrossRefGoogle Scholar
  69. Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71CrossRefGoogle Scholar
  70. Lantz H, Johnston P, Park D, Minter DW (2011) Molecular phylogeny reveals a core clade of Rhytismatales. Mycologia 103:57–74PubMedCrossRefGoogle Scholar
  71. Lee B-H, Eo J-K, Eom A-H (2016a) Notes on five endophytic fungal species isolated from needle leaves of conifers in Korea. Korean J Mycol 44:51–56CrossRefGoogle Scholar
  72. Lee HB, Mun HY, Nguyen TTT, Kim J-C, Stone JK (2016b) Abieticola koreana gen. et sp. nov., a griseofulvin-producing endophytic xylariaceous ascomycete from Korea. Mycotaxon 131:749–764CrossRefGoogle Scholar
  73. Leuchtmann A, Clay K (1993) Nonreciprocal compatibility between Epichloë typhina and four host grasses. Mycologia 85:157–163CrossRefGoogle Scholar
  74. Lindner DL, Carlsen T, Henrik Nilsson R, Davey M, Schumacher T, Kauserud H (2013) Employing 454 amplicon pyrosequencing to reveal intragenomic divergence in the internal transcribed spacer rDNA region in fungi. Ecol Evolut 3:1751–1764CrossRefGoogle Scholar
  75. Liu K-L, Porras-Alfaro A, Kuske CR, Eichorst SA, Xie G (2012) Accurate, rapid taxonomic classification of fungal large-subunit rRNA genes. Appl Environ Microbiol 78:1523–1533PubMedPubMedCentralCrossRefGoogle Scholar
  76. Livsey S, Barklund P (1992) Lophodermium piceae and Rhizosphaera kalkhoffii in fallen needles of Norway spruce (Picea abies). Eur J For Path 22:204–216CrossRefGoogle Scholar
  77. Livsey S, Minter D (1994) The taxonomy and biology of Tryblidiopsis pinastri. Can J Bot 72:549–557CrossRefGoogle Scholar
  78. Loo J, Ives N (2003) The Acadian forest: historical condition and human impacts. Forest Chronicle 79:462–474CrossRefGoogle Scholar
  79. Lorimer CG (1977) The presettlement forest and natural disturbance cycle of northeastern Maine. Ecology 58:139–148CrossRefGoogle Scholar
  80. Maloy OC (1997) White pine blister rust control in North America: a case history. Annu Rev Phytopathol 35:87–109PubMedPubMedCentralCrossRefGoogle Scholar
  81. Manter DK, Bond BJ, Kavanagh KL, Rosso PH, Filip GM (2000) Pseudothecia of Swiss needle cast fungus, Phaeocryptopus gaeumannii, physically block stomata of Douglas fir, reducing CO2 assimilation. New Phytol 148:481–491CrossRefGoogle Scholar
  82. Martin R, Gazis R, Skaltsas D, Chaverri P, Hibbett D (2015) Unexpected diversity of basidiomycetous endophytes in sapwood and leaves of Hevea. Mycologia 107:284–297PubMedCrossRefGoogle Scholar
  83. McMullin DR, Nsiama TK, Miller JD (2014) Secondary metabolites from Penicillium corylophilum isolated from damp buildings. Mycologia 106:621–628PubMedCrossRefGoogle Scholar
  84. McMullin DR, Green BD, Miller JD (2015) Antifungal sesquiterpenoids and macrolides from an endophytic Lophodermium species of Pinus strobus. Phytochem Lett 14:148–152CrossRefGoogle Scholar
  85. McMullin DR, Green BD, Prince NC, Tanney JB, Miller JD (2017a) Natural products of Picea endophytes from the Acadian forest. J Nat Prod 80:1475–1483PubMedCrossRefGoogle Scholar
  86. McMullin DR, Nguyen HDT, Daly GJ, Menard BS, Miller JD (2017b) Detection of foliar endophytes and their metabolites in Picea and Pinus seedling needles. Fungal Ecol 31:1–8Google Scholar
  87. Menkis A, Allmer J, Vasiliauskas R, Lygis V, Stenlid J, Finlay R (2004) Ecology and molecular characterization of dark septate fungi from roots, living stems, coarse and fine woody debris. Mycol Res 108:965–973PubMedPubMedCentralCrossRefGoogle Scholar
  88. Miller JD (1986) Toxins of endophytic and epiphytic fungi of conifer needles. In: Fokkema NJ, Van Huevel J (eds) Microbiology of the phyllosphere. Cambridge University Press, Cambridge, pp 223–231Google Scholar
  89. Miller JD (2011) Foliar endophytes of spruce species found in the Acadian forest: basis and potential for improving the tolerance of the forest to spruce budworm. In: Endophytes of Forest Trees. Springer, Berlin, pp 237–249Google Scholar
  90. Miller JD, Sumarah MW, Adams GW (2008) Effect of a rugulosin-producing endophyte in Picea glauca on Choristoneura fumiferana. J Chem Ecol 34:362–368PubMedPubMedCentralCrossRefGoogle Scholar
  91. Miller JD, Cherid H, Sumarah MW, Adams GW (2009) Horizontal transmission of the Picea glauca foliar endophyte Phialocephala scopiformis CBS 120377. Fungal Ecol 2:98–101CrossRefGoogle Scholar
  92. Mitchell C, Williamson B, Millar C (1976) Hendersonia acicola on pine needles infected by Lophodermella sulcigena. For Pathol 6:92–102CrossRefGoogle Scholar
  93. Monnet F, Vaillant N, Hitmi A, Coudret A, Sallanon H (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiol Plant 113:557–563CrossRefGoogle Scholar
  94. Mosseler A, Lynds J, Major J (2003a) Old-growth forests of the Acadian Forest Region. Environ Rev 11:S47–S77CrossRefGoogle Scholar
  95. Mosseler A, Major J, Rajora O (2003b) Old-growth red spruce forests as reservoirs of genetic diversity and reproductive fitness. Theor Appl Genet 106:931–937PubMedCrossRefGoogle Scholar
  96. Napier EJ, Turner DI, Rhodes A (1956) The in vitro action of griseofulvin against pathogenic fungi of plants. Ann Bot 20:461–466CrossRefGoogle Scholar
  97. National Forestry Database (2017) Forest insects: spruce budworm, 1975–2015. Accessed: April 27, 2018.
  98. Natural Resources Canada (2012) White pine blister rust fact sheet. Retrieved 25 Sept 2017, from http://www.tidcfnrcangcca/diseases/factsheet/24
  99. Nielsen KF, Sumarah MW, Frisvad JC, Miller JD (2006) Production of metabolites from the Penicillium roqueforti complex. J Agric Food Chem 54:3756–3763PubMedCrossRefGoogle Scholar
  100. Noble HM, Langley D, Sidebottom P, Lane S, Fisher P (1991) An echinocandin from an endophytic Cryptosporiopsis sp. and Pezicula sp. in Pinus sylvestris and Fagus sylvatica. Mycol Res 95:1439–1440CrossRefGoogle Scholar
  101. Okane I, Srikitikulchai P, Toyama K, Læssøe T, Sivichai S, Hywel-Jones N, Nakagiri A, Potacharoen W, K-i Suzuki (2008) Study of endophytic Xylariaceae in Thailand: diversity and taxonomy inferred from rDNA sequence analyses with saprobes forming fruit bodies in the field. Mycoscience 49:359–372CrossRefGoogle Scholar
  102. Oono R, Lefèvre E, Simha A, Lutzoni F (2015) A comparison of the community diversity of foliar fungal endophytes between seedling and adult loblolly pines (Pinus taeda). Fungal Biol 119:917–928PubMedPubMedCentralCrossRefGoogle Scholar
  103. Osono T, Tateno O, Masuya H (2013) Diversity and ubiquity of xylariaceous endophytes in live and dead leaves of temperate forest trees. Mycoscience 54:54–61CrossRefGoogle Scholar
  104. Osorio M, Stephan BR (1991) Life cycle of Lophodermium piceae in Norway spruce needles. Eur J For Path 21:152–163CrossRefGoogle Scholar
  105. Park JH, Choi G, Lee HB, Kim K, Jung HS, Lee S-W, Jang KS, Cho KY, Kim J-C (2005) Griseofulvin from Xylaria sp. strain F0010, an endophytic fungus of Abies holophylla and its antifungal activity against plant pathogenic fungi. J Microbiol Biotechnol 15:112–117Google Scholar
  106. Petrini L, Petrini O (1985) Xylariaceous fungi as endophytes. Sydowia 38:216–234Google Scholar
  107. Petrini O, Petrini L, Rodrigues K (1995) Xylariaceous endophytes: an exercise in biodiversity. Fitopatol Bras 20:531–539Google Scholar
  108. Pirttilä AM, Frank C (2011) Endophytes of forest trees: biology and applications. Springer, BerlinCrossRefGoogle Scholar
  109. Porter TM, Golding GB (2012) Factors that affect large subunit ribosomal DNA amplicon sequencing studies of fungal communities: classification method, primer choice, and error. PLoS ONE 7(4):e35749PubMedPubMedCentralCrossRefGoogle Scholar
  110. Prihatini I, Glen M, Wardlaw TJ, Mohammed CL (2016) Diversity and identification of fungi associated with needles of Pinus radiata in Tasmania. South Forest: J For Sci 78:19–34CrossRefGoogle Scholar
  111. Prior R, Görges K, Yurkov A, Begerow D (2014) New isolation method for endophytes based on enzyme digestion. Mycol Prog 13:849–856CrossRefGoogle Scholar
  112. Qadri M, Rajput R, Abdin MZ, Vishwakarma RA, Riyaz-Ul-Hassan S (2014) Diversity, molecular phylogeny, and bioactive potential of fungal endophytes associated with the Himalayan blue pine (Pinus wallichiana). Microb Ecol 67:877–887PubMedCrossRefGoogle Scholar
  113. Raja HA, Miller AN, Pearce CJ, Oberlies NH (2017) Fungal identification using molecular tools: a primer for the natural products research community. J Nat Prod 80:756–770PubMedPubMedCentralCrossRefGoogle Scholar
  114. Rehner SA, Uecker FA (1994) Nuclear ribosomal internal transcribed spacer phylogeny and host diversity in the coelomycete Phomopsis. Can J Bot 72:1666–1674CrossRefGoogle Scholar
  115. Reich PB, Oleksyn J, Modrzynski J, Tjoelker MG (1996) Evidence that longer needle retention of spruce and pine populations at high elevations and high latitudes is largely a phenotypic response. Tree Physiol 16:643–647PubMedCrossRefGoogle Scholar
  116. Reignoux SN, Green S, Ennos RA (2014) Molecular identification and relative abundance of cryptic Lophodermium species in natural populations of Scots pine, Pinus sylvestris L. Fungal Biol 118:835–845PubMedCrossRefGoogle Scholar
  117. Révay Á, Gönczöl J (2010) Rainborne hyphomycete conidia from evergreen trees. Nova Hedwig 91:151–163CrossRefGoogle Scholar
  118. Révay Á, Gönczöl J (2011) Canopy fungi (“terrestrial aquatic hyphomycetes”) from twigs of living evergreen and deciduous trees in Hungary. Nova Hedwig 92:303–316CrossRefGoogle Scholar
  119. Rice J, Pinkerton B, Stringer W, Undersander D (1990) Seed production in tall fescue as affected by fungal endophyte. Crop Sci 30:1303–1305CrossRefGoogle Scholar
  120. Richardson SN, Walker AK, Nsiama TK, McFarlane J, Sumarah MW, Ibrahim A, Miller JD (2014) Griseofulvin-producing Xylaria endophytes of Pinus strobus and Vaccinium angustifolium: evidence for a conifer-understory species endophyte ecology. Fungal Ecol 11:107–113CrossRefGoogle Scholar
  121. Richardson SN, Nsiama TK, Walker AK, McMullin DR, Miller JD (2015) Antimicrobial dihydrobenzofurans and xanthenes from a foliar endophyte of Pinus strobus. Phytochemistry 117:436–443PubMedPubMedCentralCrossRefGoogle Scholar
  122. Rocha AC, Garcia D, Uetanabaro AP, Carneiro RT, Araújo IS, Mattos CR, Góes-Neto A (2011) Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Divers 47:75–84CrossRefGoogle Scholar
  123. Rodriguez R, White J Jr, Arnold A, Redman R (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedPubMedCentralCrossRefGoogle Scholar
  124. Royama TO (1984) Population dynamics of the spruce budworm Choristoneura fumiferana. Ecological Mon 54:429–462CrossRefGoogle Scholar
  125. Royama TO, MacKinnon WE, Kettela EG, Carter NE, Hartling LK (2005) Analysis of spruce budworm outbreak cycles in New Brunswick, Canada, since 1952. Ecology 86:1212–1224CrossRefGoogle Scholar
  126. Samson RA, Visagie CM, Houbraken J, Hong S-B, Hubka V, Klaassen CH, Perrone G, Seifert KA, Susca A, Tanney JB (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173PubMedPubMedCentralCrossRefGoogle Scholar
  127. Sati S, Belwal M (2005) Aquatic hyphomycetes as endophytes of riparian plant roots. Mycologia 97:45–49PubMedCrossRefGoogle Scholar
  128. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bolchacova E, Voigt K, Crous PW (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109:6241–6246PubMedPubMedCentralCrossRefGoogle Scholar
  129. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedCrossRefGoogle Scholar
  130. Schulz B, Sucker J, Aust H, Krohn K, Ludewig K, Jones P, Döring D (1995) Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res 99:1007–1015CrossRefGoogle Scholar
  131. Selosse MA, Vohník M, Chauvet E (2008) Out of the rivers: are some aquatic hyphomycetes plant endophytes? New Phytol 178:3–7PubMedCrossRefPubMedCentralGoogle Scholar
  132. Sherwood MA (1980) Taxonomic studies in the Phacidiales: the genus Coccomyces (Rhytismataceae). Occas Pap Farlow Herbarium Cryptogamic Bot 15:1–120Google Scholar
  133. Sica VP, Rees ER, Tchegnon E, Bardsley RH, Raja HA, Oberlies NH (2016) Spatial and temporal profiling of griseofulvin production in Xylaria cubensis using mass spectrometry mapping. Front Microbiol 7:544PubMedPubMedCentralCrossRefGoogle Scholar
  134. Sieber TN (2002) Fungal root endophytes. Plant roots: the hidden half. Marcel Dekker, New York, pp 887–917CrossRefGoogle Scholar
  135. Sieber T, Sieber-Canavesi F, Dorworth C (1991) Endophytic fungi of red alder (Alnus rubra) leaves and twigs in British Columbia. Can J Bot 69:407–411CrossRefGoogle Scholar
  136. Siegel M, Latch G, Bush L, Fannin F, Rowan D, Tapper B, Bacon C, Johnson M (1990) Fungal endophyte-infected grasses: alkaloid accumulation and aphid response. J Chem Ecol 16:3301–3315PubMedPubMedCentralCrossRefGoogle Scholar
  137. Sigler L, Allan T, Lim SR, Berch S, Berbee M (2005) Two new Cryptosporiopsis species from roots of ericaceous hosts in western North America. Stud Mycol 53:53–62CrossRefGoogle Scholar
  138. Sokolski S, Piché Y, Bérubé JA (2004) Lophodermium macci sp. nov., a new species on senesced foliage of five-needle pines. Mycologia 96:1261–1267PubMedCrossRefPubMedCentralGoogle Scholar
  139. Sokolski S, Piche Y, Chauvet É, Bérubé JA (2006a) A fungal endophyte of black spruce (Picea mariana) needles is also an aquatic hyphomycete. Mol Ecol 15:1955–1962PubMedCrossRefPubMedCentralGoogle Scholar
  140. Sokolski S, Piché Y, Laitung B, Bérubé J (2006b) Streams in Quebec boreal and mixed-wood forests reveal a new aquatic hyphomycete species, Dwayaangam colodena sp. nov. Mycologia 98:628–636PubMedCrossRefGoogle Scholar
  141. Solheim H, Torp TB, Hietala AM (2013) Characterization of the ascomycetes Therrya fuckelii and T. pini fruiting on Scots pine branches in Nordic countries. Mycol Prog 12:37–44CrossRefGoogle Scholar
  142. Song M, Li X, Saikkonen K, Li C, Nan Z (2015) An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecol 13:44–52CrossRefGoogle Scholar
  143. Sridhar K, Bärlocher F (1992) Endophytic aquatic hyphomycetes of roots of spruce, birch and maple. Mycol Res 96:305–308CrossRefGoogle Scholar
  144. Sridhar K, Karamchand K (2009) Diversity of water-borne fungi in stemflow and throughfall of tree canopies in India. Sydowia 61:327–344Google Scholar
  145. Stadler M (2011) Importance of secondary metabolites in the Xylariaceae as parameters for assessment of their taxonomy, phylogeny, and functional biodiversity. Curr Res Environ Appl Mycol 1:75–133CrossRefGoogle Scholar
  146. Staley JM, Bynum HH (1972) A new Lophodermella on Pinus ponderosa and P. attenuata. Mycologia 64:722–726CrossRefGoogle Scholar
  147. Stefani F, Bérubé J (2006) Biodiversity of foliar fungal endophytes in white spruce (Picea glauca) from southern Québec. Botany 84:777–790Google Scholar
  148. Stielow J, Lévesque C, Seifert K, Meyer W, Irinyi L, Smits D, Renfurm R, Verkley G, Groenewald M, Chaduli D (2015) One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes. Persoonia 35:242–263PubMedPubMedCentralCrossRefGoogle Scholar
  149. Stillwell M, Wood F, Strunz G (1969) A broad-spectrum antibiotic produced by a species of Cryptosporiopsis. Can J Microbiol 15:501–507PubMedCrossRefGoogle Scholar
  150. Stone JK, Sherwood MA, Carroll GC (1996) Canopy microfungi: function and diversity. Northwest Sci 70:37–45Google Scholar
  151. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502PubMedPubMedCentralCrossRefGoogle Scholar
  152. Strobel GA, Miller RV, Martinez-Miller C, Condron MM, Teplow DB, Hess W (1999) Cryptocandin, a potent antimycotic from the endophytic fungus Cryptosporiopsis cf. quercina. Microbiology 145:1919–1926PubMedCrossRefPubMedCentralGoogle Scholar
  153. Strongman DB, Strunz GM, Giguère P, Yu C-M, Calhoun L (1988) Enniatins from Fusarium avenaceum isolated from balsam fir foliage and their toxicity to spruce budworm larvae, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). J Chem Ecol 14:753–764PubMedCrossRefPubMedCentralGoogle Scholar
  154. Strunz G, Court A, Komlossy J, Stillwell M (1969) Cryptosporiopsin, an amended structure. Can J Chem 47:3700–3701CrossRefGoogle Scholar
  155. Sumarah MW, Miller JD, Adams GW (2005) Measurement of a rugulosin-producing endophyte in white spruce seedlings. Mycologia 97:770–776PubMedCrossRefPubMedCentralGoogle Scholar
  156. Sumarah MW, Adams GW, Berghout J, Slack GJ, Wilson AM, Miller JD (2008a) Spread and persistence of a rugulosin-producing endophyte in Picea glauca seedlings. Mycol Res 112:731–736PubMedPubMedCentralCrossRefGoogle Scholar
  157. Sumarah MW, Puniani E, Blackwell BA, Miller JD (2008b) Characterization of polyketide metabolites from foliar endophytes of Picea glauca. J Nat Prod 71:1393–1398PubMedPubMedCentralCrossRefGoogle Scholar
  158. Sumarah MW, Miller JD (2009) Anti-insect secondary metabolites from fungal endophytes of conifer trees. Nat Prod Commun 4:1497–1504PubMedGoogle Scholar
  159. Sumarah MW, Kesting JR, Sørensen D, Miller JD (2011) Antifungal metabolites from fungal endophytes of Pinus strobus. Phytochemistry 72:1833–1837PubMedCrossRefGoogle Scholar
  160. Sumarah MW, Puniani E, Sørensen D, Blackwell BA, Miller JD (2010) Secondary metabolites from anti-insect extracts of endophytic fungi isolated from Picea rubens. Phytochemistry 71:760–765PubMedPubMedCentralCrossRefGoogle Scholar
  161. Sumarah MW, Walker AK, Seifert KA, Todorov A, Miller JD (2015) Screening of fungal endophytes isolated from eastern white pine needles. The formation, structure and activity of phytochemicals. Springer, Berlin, pp 195–206CrossRefGoogle Scholar
  162. Suske J, Acker G (1989) Identification of endophytic hyphae of Lophodermium piceae in tissues of green, symptomless Norway spruce needles by immunoelectron microscopy. Can J Bot 67:1768–1774CrossRefGoogle Scholar
  163. Sy-Cordero AA, Pearce CJ, Oberlies NH (2012) Revisiting the enniatins: a review of their isolation, biosynthesis, structure determination, and biological activities. J Antibiot 65:541PubMedPubMedCentralCrossRefGoogle Scholar
  164. Tanney JB (2016) A taxonomic and phylogenetic investigation of conifer endophytes of Eastern Canada. PhD Thesis. Department of Biology. Carleton University, OttawaGoogle Scholar
  165. Tanney JB, Douglas B, Seifert KA (2016a) Sexual and asexual states of some endophytic Phialocephala species of Picea. Mycologia: 15–136Google Scholar
  166. Tanney JB, McMullin DR, Green BD, Miller JD, Seifert KA (2016b) Production of antifungal and antiinsectan metabolites by the Picea endophyte Diaporthe maritima sp. nov. Fungal Biol 120:1448–1457PubMedCrossRefPubMedCentralGoogle Scholar
  167. Tanney JB, Seifert KA (2017) Lophodermium resinosum sp. nov. from red pine (Pinus resinosa) in Eastern Canada. Botany 95:773–784CrossRefGoogle Scholar
  168. Tedersoo L, Lindahl B (2016) Fungal identification biases in microbiome projects. Environ Microbiol Rep 8:774–779CrossRefGoogle Scholar
  169. Thiéry O, Moora M, Vasar M, Zobel M, Öpik M (2012) Inter-and intrasporal nuclear ribosomal gene sequence variation within one isolate of arbuscular mycorrhizal fungus, Diversispora sp. Symbiosis 58:135–147CrossRefGoogle Scholar
  170. Thiéry O, Vasar M, Jairus T, Davison J, Roux C, Kivistik PA, Metspalu A, Milani L, Saks Ü, Moora M (2016) Sequence variation in nuclear ribosomal small subunit, internal transcribed spacer and large subunit regions of Rhizophagus irregularis and Gigaspora margarita is high and isolate-dependent. Mol Ecol 25:2816–2832PubMedCrossRefPubMedCentralGoogle Scholar
  171. Thomas DC, Vandegrift R, Ludden A, Carroll GC, Roy BA (2016) Spatial ecology of the fungal genus Xylaria in a tropical cloud forest. Biotropica 48:381–393CrossRefGoogle Scholar
  172. Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Moretto A (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214:913–919PubMedPubMedCentralCrossRefGoogle Scholar
  173. U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914PubMedPubMedCentralCrossRefGoogle Scholar
  174. U’Ren JM, Miadlikowska J, Zimmerman NB, Lutzoni F, Stajich JE, Arnold AE (2016) Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota). Mol Phylogen Evol 98:210–232CrossRefGoogle Scholar
  175. Udayanga D, Castlebury LA, Rossman AY, Chukeatirote E, Hyde KD (2014) Insights into the genus Diaporthe: phylogenetic species delimitation in the D. eres species complex. Fungal Divers 67:203–229CrossRefGoogle Scholar
  176. van Dijk EL, Jaszczyszyn Y, Thermes C (2014) Library preparation methods for next-generation sequencing: tone down the bias. Exp Cell Res 322:12–20PubMedCrossRefGoogle Scholar
  177. Verkley G (1999) A monograph of the genus Pezicula and its anamorphs. Stud Mycol 44:5–171Google Scholar
  178. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedPubMedCentralCrossRefGoogle Scholar
  179. Visagie CM, Houbraken J, Frisvad JC, Hong S-B, Klaassen CHW, Perrone G, Seifert KA, Varga J, Yaguchi J, Samson RA (2014) Identification and nomenclature of the genus Penicillium. Stud Mycol 78:343–371PubMedPubMedCentralCrossRefGoogle Scholar
  180. Vrålstad T (2011) ITS, OTUs and beyond—fungal hyperdiversity calls for supplementary solutions. Mol Ecol 20:2873–2875PubMedCrossRefGoogle Scholar
  181. Wang S, Cannon P, Li Z-J, Hou C-L (2014) Multigene phylogenetic analysis detects cryptic species of Tryblidiopsis in China. Mycologia 106:95–104PubMedCrossRefGoogle Scholar
  182. Webber J (1981) A natural biological control of Dutch elm disease. Nature 292:449–451CrossRefGoogle Scholar
  183. Webber J, Gibbs JN (1984) Colonization of elm bark by Phomopsis oblonga. Trans Br Mycol Soc 82:348–352CrossRefGoogle Scholar
  184. Webster J (1959) Experiments with spores of aquatic hyphomycetes. I. Sedimentation and impaction on smooth surfaces. Ann Bot 23:595–611CrossRefGoogle Scholar
  185. Wein RW, Moore JM (1977) Fire history and rotations in the New Brunswick Acadian Forest. Can J For Res 7:285–294CrossRefGoogle Scholar
  186. Whalley AJS, Edwards RL (1995) Secondary metabolites and systematic arrangement within the Xylariaceae. Can J Bot 73(S1):802–810CrossRefGoogle Scholar
  187. Wilson RW, Wheatcroft RGC, Miller JD, Whitney NJ (1994) Genetic diversity among natural populations of endophytic Lophodermium pinastri from Pinus resinosa. Mycol Res 98:740–744CrossRefGoogle Scholar
  188. Winton LM, Stone JK, Hansen EM, Shoemaker R (2007) The systematic position of Phaeocryptopus gaeumannii. Mycologia 99:240–252PubMedCrossRefGoogle Scholar
  189. Xia C, Zhang X, Christensen MJ, Nan Z, Li C (2015) Epichloë endophyte affects the ability of powdery mildew (Blumeria graminis) to colonise drunken horse grass (Achnatherum inebrians). Fungal Ecol 16:26–33CrossRefGoogle Scholar
  190. Yang Q, Fan X, Du Z, Tian C (2017) Diaporthe juglandicola sp. nov. (Diaporthales, Ascomycetes), evidenced by morphological characters and phylogenetic analysis. Mycosphere 8:817–826CrossRefGoogle Scholar
  191. Yuan Z-L, Rao L-B, Chen Y-C, Zhang C-L, Wu Y-G (2011) From pattern to process: species and functional diversity in fungal endophytes of Abies beshanzuensis. Fungal Biol 115:197–213PubMedCrossRefGoogle Scholar
  192. Yuan Z, Verkley GJ (2015) Pezicula neosporulosa sp. nov. (Helotiales, Ascomycota), an endophytic fungus associated with Abies spp. in China and Europe. Mycoscience 56:205–213CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Joey B. Tanney
    • 1
  • David R. McMullin
    • 2
  • J. David Miller
    • 2
  1. 1.Department of BiologyCarleton UniversityOttawaCanada
  2. 2.Department of ChemistryCarleton UniversityOttawaCanada

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