Skip to main content

Toxigenic Foliar Endophytes from the Acadian Forest

  • Chapter
  • First Online:
Endophytes of Forest Trees

Part of the book series: Forestry Sciences ((FOSC,volume 86))

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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 186:281–285

    PubMed  Google Scholar 

  • Allen E, Humble L (2002) Nonindigenous species introductions: a threat to Canada’s forests and forest economy. Can J Plant Path 24:103–110

    Article  Google Scholar 

  • 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 41:1–16

    Article  Google Scholar 

  • 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 40:1–12

    Article  Google Scholar 

  • Ando K (1992) A study of terrestrial aquatic hyphomycetes. Trans Mycol Soc Jpn 33:415–425

    Google Scholar 

  • Anke H, Stadler M, Mayer A, Sterner O (1995) Secondary metabolites with nematicidal and antimicrobial activity from nematophagous fungi and Ascomycetes. Can J Bot 73:932–939

    Article  Google Scholar 

  • Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549

    Article  PubMed  Google Scholar 

  • 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 100:15649–15654

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 17:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Bandoni RJ, Koske RE (1974) Monolayers and microbial dispersal. Science 183:1079–1081

    Article  PubMed  CAS  Google Scholar 

  • Barengo N, Sieber TN, Holdenrieder O (2000) Diversity of endophytic mycobiota in leaves and twigs of pubescent birch (Betula pubescens). Sydowia 52:305–320

    Google Scholar 

  • Barklund P (1987) Occurrence and pathogenicity of Lophodermium piceae appearing as an endophyte in needles of Picea abies. Trans Br Mycol Soc 89:307–313

    Article  Google Scholar 

  • Barklund P, Kowalski T (1996) Endophytic fungi in branches of Norway spruce with particular reference to Tryblidiopsis pinastri. Can J Bot 74:673–678

    Article  Google Scholar 

  • 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:e46687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blais J (1983) Trends in the frequency, extent, and severity of spruce budworm outbreaks in eastern Canada. Can J For Res 13:539–547

    Article  Google Scholar 

  • Botella L, Diez JJ (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18

    Article  Google Scholar 

  • 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 6:4088–4104

    Article  Google Scholar 

  • Butin VH, Kowalski T (1990) Die natürliche Astreinigung und ihre biologischen Voraussetzungen V. Die Pilzflor.von Fichte, Kiefer und Lärche. Eur J For Pathol 20:44–54

    Article  Google Scholar 

  • Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286

    Article  Google Scholar 

  • Carroll GC (1999) The foraging ascomycete. In: 16th International Botanical Congress, St. Louis, MO, USA

    Google Scholar 

  • 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 42:490–505

    Article  Google Scholar 

  • Chauvet E, Cornut J, Sridhar KR, Selosse M-A, Bärlocher F (2016) Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecol 19:112–127

    Article  Google Scholar 

  • 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 4:94–102

    Article  Google Scholar 

  • 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 120:1291–1322

    Article  PubMed  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Claydon N, Grove JF, Pople M (1985) Elm bark beetle boring and feeding deterrents from Phomopsis oblonga. Phytochemistry 24:937–943

    Article  CAS  Google Scholar 

  • Czabator F, Staley J, Snow G (1971) Extensive southern pine needle blight during 1970–1971, and associated fungi. Plant Dis Rep 55:764–766

    Google Scholar 

  • Darker GD (1967) A revision of the genera of the Hypodermataceae. Can J Bot 45:1399–1444

    Article  Google Scholar 

  • Davis EC, Franklin JB, Shaw AJ, Vilgalys R (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 90:1661–1667

    Article  PubMed  Google Scholar 

  • 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 120:1323–1340

    Article  PubMed  Google Scholar 

  • 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 105:991–997

    Article  Google Scholar 

  • Dreyfuss M, Petrini O (1984) Further investigations on the occurrence and distribution of endophytic fungi in tropical plants. Bot Helv 94:33–40

    Google Scholar 

  • 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 13:917–931

    Article  CAS  Google Scholar 

  • 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 35:1965–1977

    Article  Google Scholar 

  • 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 21:509–524

    Article  Google Scholar 

  • Et-Touil K, Bernier L, Beaulieu J, Bérubé J, Hopkin A, Hamelin R (1999) Genetic structure of Cronartium ribicola populations in eastern Canada. Phytopathology 89:915–919

    Article  PubMed  CAS  Google Scholar 

  • Farr D, Rossman A (2016). Fungal Databases, Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved 25 Sept 2017, from http://nt.ars-grin.gov/fungaldatabases/

  • Findlay JA, Buthelezi S, Lavoie R, Peña-Rodriguez L, Miller JD (1995) Bioactive isocoumarins and related metabolites from conifer endophytes. J Nat Prod 58:1759–1766

    Article  PubMed  CAS  Google Scholar 

  • Findlay JA, Li G, Miller JD, Womiloju TO (2003) Insect toxins from spruce endophytes. Can J Chem 81:284–292

    Article  CAS  Google Scholar 

  • Fleming RA, Candau J-N, McAlpine RS (2002) Landscape-scale analysis of interactions between insect defoliation and forest fire in central Canada. Clim Change 55:251–272

    Article  Google Scholar 

  • 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 44:1138–1143

    Article  CAS  Google Scholar 

  • Gao Y, Liu F, Cai L (2016) Unravelling Diaporthe species associated with Camellia. Syst Biodivers 14:102–117

    Article  Google Scholar 

  • Gazis R, Rehner S, Chaverri P (2011) Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol 20:3001–3013

    Article  PubMed  Google Scholar 

  • Gönczöl J, Révay Á (2004) Fungal spores in rainwater: stemflow, throughfall and gutter conidial assemblages. Fungal Divers 16:67–86

    Google Scholar 

  • Green BD (2016). Characterization of secondary metabolites produced by foliar endophytes of red and black spruce. MSc. Thesis. Department of Chemistry, Carleton University Ottawa

    Google Scholar 

  • 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 25:1208–1212

    Article  Google Scholar 

  • 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 1:865–869

    Article  Google Scholar 

  • 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 113:207–221

    Article  PubMed  Google Scholar 

  • 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 5:479–483

    Article  PubMed  CAS  Google Scholar 

  • 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 114:901–910

    Article  PubMed  Google Scholar 

  • 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 65:899–900

    Article  Google Scholar 

  • Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11:129–133

    Article  PubMed  CAS  Google Scholar 

  • 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 108:1049–1068

    PubMed  Google Scholar 

  • 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 13:834–839

    Article  CAS  Google Scholar 

  • Horn WS, Simmonds MS, Schwartz RE, Blaney WM (1996) Variation in production of phomodiol and phomopsolide B by Phomopsis spp. Mycologia: 588–595

    Google Scholar 

  • 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 71:452–468

    Article  PubMed  Google Scholar 

  • 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 

  • 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 41:1657–1660

    Article  CAS  Google Scholar 

  • Jalkanen R, Laakso R (1986) Hendersonia acicola in an epidemic caused by Lophodermella sulcigena with special reference to biological control. Karstenia 26:49–56

    Article  Google Scholar 

  • 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 67:723–725

    Article  Google Scholar 

  • Jumpponen A, Jones K (2009) Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 184:438–448

    Article  PubMed  CAS  Google Scholar 

  • 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 22:29–40

    Article  Google Scholar 

  • 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 6:38–47

    Article  Google Scholar 

  • Kirk P, Cannon P, Minter D, Stalpers J (2008) Dictionary of the Fungi, 10th edn. CAB International, University Press, Cambridge

    Google Scholar 

  • Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous P (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35:87–100

    Article  Google Scholar 

  • Koukol O, Kolařík M, Kolářová Z, Baldrian P (2012) Diversity of foliar endophytes in wind-fallen Picea abies trees. Fungal Divers 54:69–77

    Article  Google Scholar 

  • Kowalski T, Kehr R (1992) Endophytic fungal colonization of branch bases in several forest tree species. Sydowia 44:137–168

    Google Scholar 

  • Kowalski T, Kehr R (1995) Two new species of Phialocephala occurring on Picea and Alnus. Can J Bot 73:26–32

    Article  Google Scholar 

  • Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71

    Article  Google Scholar 

  • Lantz H, Johnston P, Park D, Minter DW (2011) Molecular phylogeny reveals a core clade of Rhytismatales. Mycologia 103:57–74

    Article  PubMed  CAS  Google Scholar 

  • 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 44:51–56

    Article  Google Scholar 

  • 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 131:749–764

    Article  Google Scholar 

  • Leuchtmann A, Clay K (1993) Nonreciprocal compatibility between Epichloë typhina and four host grasses. Mycologia 85:157–163

    Article  Google Scholar 

  • 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 3:1751–1764

    Article  Google Scholar 

  • 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 78:1523–1533

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livsey S, Barklund P (1992) Lophodermium piceae and Rhizosphaera kalkhoffii in fallen needles of Norway spruce (Picea abies). Eur J For Path 22:204–216

    Article  Google Scholar 

  • Livsey S, Minter D (1994) The taxonomy and biology of Tryblidiopsis pinastri. Can J Bot 72:549–557

    Article  Google Scholar 

  • Loo J, Ives N (2003) The Acadian forest: historical condition and human impacts. Forest Chronicle 79:462–474

    Article  Google Scholar 

  • Lorimer CG (1977) The presettlement forest and natural disturbance cycle of northeastern Maine. Ecology 58:139–148

    Article  Google Scholar 

  • Maloy OC (1997) White pine blister rust control in North America: a case history. Annu Rev Phytopathol 35:87–109

    Article  PubMed  CAS  Google Scholar 

  • 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 148:481–491

    Article  CAS  PubMed  Google Scholar 

  • Martin R, Gazis R, Skaltsas D, Chaverri P, Hibbett D (2015) Unexpected diversity of basidiomycetous endophytes in sapwood and leaves of Hevea. Mycologia 107:284–297

    Article  PubMed  Google Scholar 

  • McMullin DR, Nsiama TK, Miller JD (2014) Secondary metabolites from Penicillium corylophilum isolated from damp buildings. Mycologia 106:621–628

    Article  PubMed  CAS  Google Scholar 

  • McMullin DR, Green BD, Miller JD (2015) Antifungal sesquiterpenoids and macrolides from an endophytic Lophodermium species of Pinus strobus. Phytochem Lett 14:148–152

    Article  CAS  Google Scholar 

  • McMullin DR, Green BD, Prince NC, Tanney JB, Miller JD (2017a) Natural products of Picea endophytes from the Acadian forest. J Nat Prod 80:1475–1483

    Article  PubMed  CAS  Google Scholar 

  • 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 31:1–8

    Google Scholar 

  • 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 108:965–973

    Article  PubMed  CAS  Google Scholar 

  • 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 223–231

    Google Scholar 

  • 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 237–249

    Google Scholar 

  • Miller JD, Sumarah MW, Adams GW (2008) Effect of a rugulosin-producing endophyte in Picea glauca on Choristoneura fumiferana. J Chem Ecol 34:362–368

    Article  PubMed  CAS  Google Scholar 

  • Miller JD, Cherid H, Sumarah MW, Adams GW (2009) Horizontal transmission of the Picea glauca foliar endophyte Phialocephala scopiformis CBS 120377. Fungal Ecol 2:98–101

    Article  Google Scholar 

  • Mitchell C, Williamson B, Millar C (1976) Hendersonia acicola on pine needles infected by Lophodermella sulcigena. For Pathol 6:92–102

    Article  Google Scholar 

  • Monnet F, Vaillant N, Hitmi A, Coudret A, Sallanon H (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiol Plant 113:557–563

    Article  CAS  Google Scholar 

  • Mosseler A, Lynds J, Major J (2003a) Old-growth forests of the Acadian Forest Region. Environ Rev 11:S47–S77

    Article  Google Scholar 

  • Mosseler A, Major J, Rajora O (2003b) Old-growth red spruce forests as reservoirs of genetic diversity and reproductive fitness. Theor Appl Genet 106:931–937

    Article  PubMed  CAS  Google Scholar 

  • Napier EJ, Turner DI, Rhodes A (1956) The in vitro action of griseofulvin against pathogenic fungi of plants. Ann Bot 20:461–466

    Article  CAS  Google Scholar 

  • National Forestry Database (2017) Forest insects: spruce budworm, 1975–2015. Accessed: April 27, 2018. http://nfdp.ccfm.org/data/graphs/graph_41_a_e.php

  • Natural Resources Canada (2012) White pine blister rust fact sheet. Retrieved 25 Sept 2017, from http://www.tidcfnrcangcca/diseases/factsheet/24

  • Nielsen KF, Sumarah MW, Frisvad JC, Miller JD (2006) Production of metabolites from the Penicillium roqueforti complex. J Agric Food Chem 54:3756–3763

    Article  PubMed  CAS  Google Scholar 

  • 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 95:1439–1440

    Article  CAS  Google Scholar 

  • 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 49:359–372

    Article  CAS  Google Scholar 

  • 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 119:917–928

    Article  PubMed  PubMed Central  Google Scholar 

  • Osono T, Tateno O, Masuya H (2013) Diversity and ubiquity of xylariaceous endophytes in live and dead leaves of temperate forest trees. Mycoscience 54:54–61

    Article  Google Scholar 

  • Osorio M, Stephan BR (1991) Life cycle of Lophodermium piceae in Norway spruce needles. Eur J For Path 21:152–163

    Article  Google Scholar 

  • 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 15:112–117

    CAS  Google Scholar 

  • Petrini L, Petrini O (1985) Xylariaceous fungi as endophytes. Sydowia 38:216–234

    Google Scholar 

  • Petrini O, Petrini L, Rodrigues K (1995) Xylariaceous endophytes: an exercise in biodiversity. Fitopatol Bras 20:531–539

    Google Scholar 

  • Pirttilä AM, Frank C (2011) Endophytes of forest trees: biology and applications. Springer, Berlin

    Book  Google Scholar 

  • 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):e35749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 78:19–34

    Article  Google Scholar 

  • Prior R, Görges K, Yurkov A, Begerow D (2014) New isolation method for endophytes based on enzyme digestion. Mycol Prog 13:849–856

    Article  Google Scholar 

  • 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 67:877–887

    Article  PubMed  Google Scholar 

  • 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 80:756–770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rehner SA, Uecker FA (1994) Nuclear ribosomal internal transcribed spacer phylogeny and host diversity in the coelomycete Phomopsis. Can J Bot 72:1666–1674

    Article  CAS  Google Scholar 

  • 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 16:643–647

    Article  PubMed  CAS  Google Scholar 

  • 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 118:835–845

    Article  PubMed  CAS  Google Scholar 

  • Révay Á, Gönczöl J (2010) Rainborne hyphomycete conidia from evergreen trees. Nova Hedwig 91:151–163

    Article  Google Scholar 

  • Révay Á, Gönczöl J (2011) Canopy fungi (“terrestrial aquatic hyphomycetes”) from twigs of living evergreen and deciduous trees in Hungary. Nova Hedwig 92:303–316

    Article  Google Scholar 

  • Rice J, Pinkerton B, Stringer W, Undersander D (1990) Seed production in tall fescue as affected by fungal endophyte. Crop Sci 30:1303–1305

    Article  Google Scholar 

  • 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 11:107–113

    Article  Google Scholar 

  • Richardson SN, Nsiama TK, Walker AK, McMullin DR, Miller JD (2015) Antimicrobial dihydrobenzofurans and xanthenes from a foliar endophyte of Pinus strobus. Phytochemistry 117:436–443

    Article  PubMed  CAS  Google Scholar 

  • 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 47:75–84

    Article  Google Scholar 

  • Rodriguez R, White J Jr, Arnold A, Redman R (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  PubMed  CAS  Google Scholar 

  • Royama TO (1984) Population dynamics of the spruce budworm Choristoneura fumiferana. Ecological Mon 54:429–462

    Article  Google Scholar 

  • Royama TO, MacKinnon WE, Kettela EG, Carter NE, Hartling LK (2005) Analysis of spruce budworm outbreak cycles in New Brunswick, Canada, since 1952. Ecology 86:1212–1224

    Article  Google Scholar 

  • 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 78:141–173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sati S, Belwal M (2005) Aquatic hyphomycetes as endophytes of riparian plant roots. Mycologia 97:45–49

    Article  PubMed  CAS  Google Scholar 

  • 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 109:6241–6246

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • 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 99:1007–1015

    Article  CAS  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 

  • Sherwood MA (1980) Taxonomic studies in the Phacidiales: the genus Coccomyces (Rhytismataceae). Occas Pap Farlow Herbarium Cryptogamic Bot 15:1–120

    Google Scholar 

  • 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 7:544

    Article  PubMed  PubMed Central  Google Scholar 

  • Sieber TN (2002) Fungal root endophytes. Plant roots: the hidden half. Marcel Dekker, New York, pp 887–917

    Book  Google Scholar 

  • Sieber T, Sieber-Canavesi F, Dorworth C (1991) Endophytic fungi of red alder (Alnus rubra) leaves and twigs in British Columbia. Can J Bot 69:407–411

    Article  Google Scholar 

  • 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 16:3301–3315

    Article  PubMed  CAS  Google Scholar 

  • 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 53:53–62

    Article  Google Scholar 

  • Sokolski S, Piché Y, Bérubé JA (2004) Lophodermium macci sp. nov., a new species on senesced foliage of five-needle pines. Mycologia 96:1261–1267

    Article  PubMed  CAS  Google Scholar 

  • 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 15:1955–1962

    Article  PubMed  CAS  Google Scholar 

  • 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 98:628–636

    Article  PubMed  CAS  Google Scholar 

  • 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 12:37–44

    Article  Google Scholar 

  • Song M, Li X, Saikkonen K, Li C, Nan Z (2015) An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecol 13:44–52

    Article  Google Scholar 

  • Sridhar K, Bärlocher F (1992) Endophytic aquatic hyphomycetes of roots of spruce, birch and maple. Mycol Res 96:305–308

    Article  Google Scholar 

  • Sridhar K, Karamchand K (2009) Diversity of water-borne fungi in stemflow and throughfall of tree canopies in India. Sydowia 61:327–344

    Google Scholar 

  • 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 1:75–133

    Article  Google Scholar 

  • Staley JM, Bynum HH (1972) A new Lophodermella on Pinus ponderosa and P. attenuata. Mycologia 64:722–726

    Article  Google Scholar 

  • Stefani F, Bérubé J (2006) Biodiversity of foliar fungal endophytes in white spruce (Picea glauca) from southern Québec. Botany 84:777–790

    Google Scholar 

  • 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 35:242–263

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stillwell M, Wood F, Strunz G (1969) A broad-spectrum antibiotic produced by a species of Cryptosporiopsis. Can J Microbiol 15:501–507

    Article  PubMed  CAS  Google Scholar 

  • Stone JK, Sherwood MA, Carroll GC (1996) Canopy microfungi: function and diversity. Northwest Sci 70:37–45

    Google Scholar 

  • Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 145:1919–1926

    Article  PubMed  CAS  Google Scholar 

  • 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 14:753–764

    Article  PubMed  CAS  Google Scholar 

  • Strunz G, Court A, Komlossy J, Stillwell M (1969) Cryptosporiopsin, an amended structure. Can J Chem 47:3700–3701

    Article  CAS  Google Scholar 

  • Sumarah MW, Miller JD, Adams GW (2005) Measurement of a rugulosin-producing endophyte in white spruce seedlings. Mycologia 97:770–776

    Article  PubMed  Google Scholar 

  • 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 112:731–736

    Article  PubMed  Google Scholar 

  • Sumarah MW, Puniani E, Blackwell BA, Miller JD (2008b) Characterization of polyketide metabolites from foliar endophytes of Picea glauca. J Nat Prod 71:1393–1398

    Article  PubMed  CAS  Google Scholar 

  • Sumarah MW, Miller JD (2009) Anti-insect secondary metabolites from fungal endophytes of conifer trees. Nat Prod Commun 4:1497–1504

    PubMed  CAS  Google Scholar 

  • Sumarah MW, Kesting JR, Sørensen D, Miller JD (2011) Antifungal metabolites from fungal endophytes of Pinus strobus. Phytochemistry 72:1833–1837

    Article  PubMed  CAS  Google Scholar 

  • 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 71:760–765

    Article  PubMed  CAS  Google Scholar 

  • 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 195–206

    Chapter  Google Scholar 

  • 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 67:1768–1774

    Article  Google Scholar 

  • Sy-Cordero AA, Pearce CJ, Oberlies NH (2012) Revisiting the enniatins: a review of their isolation, biosynthesis, structure determination, and biological activities. J Antibiot 65:541

    Article  CAS  Google Scholar 

  • Tanney JB (2016) A taxonomic and phylogenetic investigation of conifer endophytes of Eastern Canada. PhD Thesis. Department of Biology. Carleton University, Ottawa

    Google Scholar 

  • Tanney JB, Douglas B, Seifert KA (2016a) Sexual and asexual states of some endophytic Phialocephala species of Picea. Mycologia: 15–136

    Google Scholar 

  • 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 120:1448–1457

    Article  PubMed  CAS  Google Scholar 

  • Tanney JB, Seifert KA (2017) Lophodermium resinosum sp. nov. from red pine (Pinus resinosa) in Eastern Canada. Botany 95:773–784

    Article  CAS  Google Scholar 

  • Tedersoo L, Lindahl B (2016) Fungal identification biases in microbiome projects. Environ Microbiol Rep 8:774–779

    Article  PubMed  Google Scholar 

  • 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 58:135–147

    Article  CAS  Google Scholar 

  • 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 25:2816–2832

    Article  PubMed  CAS  Google Scholar 

  • Thomas DC, Vandegrift R, Ludden A, Carroll GC, Roy BA (2016) Spatial ecology of the fungal genus Xylaria in a tropical cloud forest. Biotropica 48:381–393

    Article  Google Scholar 

  • 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 214:913–919

    Article  PubMed  Google Scholar 

  • 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 99:898–914

    Article  PubMed  Google Scholar 

  • 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 98:210–232

    Article  Google Scholar 

  • 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 67:203–229

    Article  Google Scholar 

  • van Dijk EL, Jaszczyszyn Y, Thermes C (2014) Library preparation methods for next-generation sequencing: tone down the bias. Exp Cell Res 322:12–20

    Article  PubMed  CAS  Google Scholar 

  • Verkley G (1999) A monograph of the genus Pezicula and its anamorphs. Stud Mycol 44:5–171

    Google Scholar 

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 78:343–371

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vrålstad T (2011) ITS, OTUs and beyond—fungal hyperdiversity calls for supplementary solutions. Mol Ecol 20:2873–2875

    Article  PubMed  Google Scholar 

  • Wang S, Cannon P, Li Z-J, Hou C-L (2014) Multigene phylogenetic analysis detects cryptic species of Tryblidiopsis in China. Mycologia 106:95–104

    Article  PubMed  Google Scholar 

  • Webber J (1981) A natural biological control of Dutch elm disease. Nature 292:449–451

    Article  Google Scholar 

  • Webber J, Gibbs JN (1984) Colonization of elm bark by Phomopsis oblonga. Trans Br Mycol Soc 82:348–352

    Article  Google Scholar 

  • Webster J (1959) Experiments with spores of aquatic hyphomycetes. I. Sedimentation and impaction on smooth surfaces. Ann Bot 23:595–611

    Article  Google Scholar 

  • Wein RW, Moore JM (1977) Fire history and rotations in the New Brunswick Acadian Forest. Can J For Res 7:285–294

    Article  Google Scholar 

  • Whalley AJS, Edwards RL (1995) Secondary metabolites and systematic arrangement within the Xylariaceae. Can J Bot 73(S1):802–810

    Article  Google Scholar 

  • Wilson RW, Wheatcroft RGC, Miller JD, Whitney NJ (1994) Genetic diversity among natural populations of endophytic Lophodermium pinastri from Pinus resinosa. Mycol Res 98:740–744

    Article  Google Scholar 

  • Winton LM, Stone JK, Hansen EM, Shoemaker R (2007) The systematic position of Phaeocryptopus gaeumannii. Mycologia 99:240–252

    Article  PubMed  CAS  Google Scholar 

  • 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 16:26–33

    Article  Google Scholar 

  • Yang Q, Fan X, Du Z, Tian C (2017) Diaporthe juglandicola sp. nov. (Diaporthales, Ascomycetes), evidenced by morphological characters and phylogenetic analysis. Mycosphere 8:817–826

    Article  Google Scholar 

  • 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 115:197–213

    Article  PubMed  Google Scholar 

  • Yuan Z, Verkley GJ (2015) Pezicula neosporulosa sp. nov. (Helotiales, Ascomycota), an endophytic fungus associated with Abies spp. in China and Europe. Mycoscience 56:205–213

    Article  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. David Miller .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Tanney, J.B., McMullin, D.R., Miller, J.D. (2018). Toxigenic Foliar Endophytes from the Acadian Forest. In: Pirttilä, A., Frank, A. (eds) Endophytes of Forest Trees. Forestry Sciences, vol 86. Springer, Cham. https://doi.org/10.1007/978-3-319-89833-9_15

Download citation

Publish with us

Policies and ethics