Advertisement

Mycological Progress

, Volume 12, Issue 2, pp 291–304 | Cite as

Spatio-temporal dynamics of endophyte diversity in the canopy of European ash (Fraxinus excelsior)

  • Almut Scholtysik
  • Martin Unterseher
  • Peter Otto
  • Christian Wirth
Original Article

Abstract

Leaf-inhabiting endophytic fungi of Fraxinus excelsior growing in a floodplain forest were isolated during 2008 to investigate vertical community structure, species richness and seasonal variation. The analysis of 848 fungal endophytes from 213 leaves resulted in 50 different species. In the understorey, infection density and species richness were higher than in the crowns of mature trees throughout the whole vegetation period. Within tree crowns, sun-exposed leaves of the top canopy exhibited the lowest infection rates. Most species were rare or absent in spring and in the light crowns and frequent in autumn and the understorey. However, some species, especially the two most frequent, Alternaria infectoria and A. alternata, deviated from these patterns. Young leaves were nearly free of endophytes. Apparently, the subsequent infection and establishment of fungi strongly depend on microclimatic parameters and leaf characters, which create highly variable spatial and temporal colonisation patterns within an individual tree.

Keywords

Endophytic fungi Temperate deciduous forest Forest canopy Diversity Species richness estimation 

References

  1. Abarenkov K, Nilsson RK, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, PennanenT SR, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol 186:281–285PubMedCrossRefGoogle Scholar
  2. Allen E, Hoch H, Steadman J, Stavely R (1991) Influence of leaf surface features on spore deposition and the epiphytic growth of phytopathogenic fungi. In: Andrews J, Hirano S (eds) Microbial ecology of leaves. Springer, New York, pp 87–110CrossRefGoogle Scholar
  3. Andersen B, Sørensen JL, Nielsen KF, Gerrits van den Ende B, de Hoog S (2009) Apolyphasic approach to the taxonomy of the Alternaria infectoria species-group. Fungal Genet Biol 46:642–656Google Scholar
  4. Andrews JH (2006) Population growth and the landscape ecology of microbes on leaf surfaces. In: Bailey MJ, Lilley AK, Timms-Wilson TM, Spencer-Phillips PTN (eds) Microbial ecology of aerial plant surfaces. CAB International, Wallingford, pp 239–250CrossRefGoogle Scholar
  5. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66CrossRefGoogle Scholar
  6. Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398PubMedCrossRefGoogle Scholar
  7. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology 88:541–549PubMedCrossRefGoogle Scholar
  8. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3(4):267–274CrossRefGoogle Scholar
  9. Aveskamp MM, Gruyter de J, Woudenberg JHC, Verkley GJM, Crous PW(2010)Highlights of the Didymellaceae: a polyphasic approach to characterise Phoma and related pleosporalean genera.Stud Mycol 65:1–60Google Scholar
  10. Bahnweg G, Heller W, Stich S, Knappe C, Betz G, Heerdt C, Kehr RD, Ernst D, Langebartels C, Nunn AJ, Rothenburger J, Schubert R, Walli P, Müller-Starck G, Werner H, Matyssek R, Sandermann H (2005) Beech leaf colonization by the endophyte Apiognomonia errabunda dramatically depends on light exposure and climatic conditions. Plant Biol 7(6):659–669PubMedCrossRefGoogle Scholar
  11. Bailey MJ, Lilley AK, Timms-Wilson TM, Spencer-Phillips PTN (2006) Microbial ecology of aerial plant surfaces. CAB International, WallingfordCrossRefGoogle Scholar
  12. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456PubMedCrossRefGoogle Scholar
  13. Chao A (1987) Estimating the population-size for capture recapture data with unequal catchability. Biometrics 43(4):783–791PubMedCrossRefGoogle Scholar
  14. 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
  15. Collado J, Platas G, Paulus B, Bills GF (2007) High-throughput culturing of fungi from plant litter by a dilution-to-extinction technique. FEMS Microbiol Ecol 60:521–533PubMedCrossRefGoogle Scholar
  16. Colwell R (2006) EstimateS: Statistical estimation of species richness and shared species from samples, Version 8.2. Persistent URL <purl.oclc.org/estimates>
  17. Crous PW, Schubert K, Braun U, et al (2007) Opportunistic, humanpathogenic species in the Herpotrichiellaceae arephenotypically similar to saprobic or phytopathogenic species in the Venturiaceae. Stud Mycol 58:185–217Google Scholar
  18. Devarajan PT, Suryanarayanan TS (2006) Evidence for the role of phytophagous insects in dispersal of non-grass fungal endophytes. Fungal Divers 23:111–119Google Scholar
  19. Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi, 2 edn. Academic, LondonGoogle Scholar
  20. Doty LS (2011) Growth-promoting endophytic fungi of forest trees. In: Pirttilä AM, Frank C (eds) Endophytes of forest trees: biology and applications. Forestry Series. Springer, Berlin, pp 151–156CrossRefGoogle Scholar
  21. Doyle JJ, Doyle JL (1987) DNA isolation from small amounts of plant tissue. Phytochemical Bull 19:11–15Google Scholar
  22. Ellis MB (1971) Dematiaceous hyphomycetes. Cambrian News, AberystwythGoogle Scholar
  23. Espinosa-Garcia F, Langenheim J (1990) The Endophytic Fungal Community In Leaves of A Coastal Redwood Population - Diversity and Spatial Patterns. New Phytol 116(1):89–97CrossRefGoogle Scholar
  24. Fan Y-M, Huang W-M, Li W, Zhang G-X (2009) Onychomycosis Caused by Nigrospora sphaerica in an immunocompetent man. Arch Dermatol 145:611–612Google Scholar
  25. Feldman T, O’Brien H, Arnold AE (2008) Moths that Vector a Plant Pathogen also Transport Endophytic Fungi and Mycoparasitic Antagonists. Microb Ecol 56:742–750PubMedCrossRefGoogle Scholar
  26. Fischer MWF, Stolze-Rybczynski JL, Cui YL, Money NP (2010) How far and how fast can mushroom spores fly? Physical limits on ballistospore size and discharge distance in the Basidiomycota. Fungal Biol 114:669–675PubMedCrossRefGoogle Scholar
  27. Gange AC (1996) Positive effects of endophyte infection on sycamore aphids. Oikos 75(3):500–510CrossRefGoogle Scholar
  28. Gilbert GS, Reynolds DR, Bethancourt A (2007) The patchiness of epifoliar fungi in tropical forests: Host range, host abundance, and environment. Ecology 88:575–581PubMedCrossRefGoogle Scholar
  29. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4(4):379–391CrossRefGoogle Scholar
  30. Grünig CR, Queloz V, Sieber TN (2011) Structure of diversity in dark septate endophytes: from species to genes. In: Pirttilä AM, Frank C (eds) Endophytes of forest trees: biology and applications. Forestry Series. Springer, Berlin, pp 3–30CrossRefGoogle Scholar
  31. Halmschlager E, Butin H, Donaubauer E (1993) Endophytic fungi in leaves and twigs of Quercus petraea. Eur J For Pathol 23(1):51–63CrossRefGoogle Scholar
  32. Hanada RE, Pomella AWV, Costa HS, Bezerra JL, Loguercio LL, Pereira JO (2010) Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuacu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biol 114:901–910PubMedCrossRefGoogle Scholar
  33. Hashizume Y, Fukuda K, Sahashi N (2010) Effects of summer temperature on fungal endophyte assemblages in Japanese beech (Fagus crenata) leaves in pure beech stands. Botany 88(3):266–274CrossRefGoogle Scholar
  34. Helander M, Wäli P, Kuuluvainen T, Saikkonen K (2006) Birch leaf endophytes in managed and natural boreal forests. Can J For Res 36(12):3239–3245CrossRefGoogle Scholar
  35. Helander M, Ahlholm J, Sieber TN, Hinneri S, Saikkonen K (2007) Fragmented environment affects birch leaf endophytes. New Phytol 175(3):547–553PubMedCrossRefGoogle Scholar
  36. Huelsenbeck JP, Ronquist F (2001) MrBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755PubMedCrossRefGoogle Scholar
  37. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  38. Johnston PR, Sutherland PW, Joshee S (2006) Visualising endophytic fungi within leaves by detection of (1-3)-ß-D-glucans in fungal cell walls. Mycologist 20:159–162CrossRefGoogle Scholar
  39. Jumpponen A, Jones KL (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513PubMedCrossRefGoogle Scholar
  40. Kowalski T, Kehr RD (1992) Endophytic fungal colonization of branch bases in several forest tree species. Sydowia 44:137–168Google Scholar
  41. Kumar S, Filipski A (2007) Multiple sequence alignment: In pursuit of homologous DNA positions. Genome Res 17(2):127–135PubMedCrossRefGoogle Scholar
  42. Lacap DC, Hyde KD, Liew ECY (2003) An evaluation of the fungal ’morphotype’ concept based on ribosomal DNA sequences. Fungal Divers 12:53–66Google Scholar
  43. Lodge DJ, Fisher PJ, Sutton BC (1996) Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycologia 88(5):733–738CrossRefGoogle Scholar
  44. Lygis V, Vasiliauskas R, Larsson KH, Stenlid J (2005) Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands of northern Lithuania, with particular reference to Armillaria cepistipes. Scand J For Res 20(4):337–346CrossRefGoogle Scholar
  45. Nilsson RH, Veldre V, Hartmann M, Unterseher M, Amend A, Bergsten J, Kristiansson E, Ryberg M, Jumpponen A, Abarenkov K (2010) An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol 3(4):284–287CrossRefGoogle Scholar
  46. Nylander J (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  47. Olbrich M, Knappe C, Wenig M, Gerstner E, Haeberle KH et al (2010) Ozone fumigation (twice ambient) reduces leaf infestation following natural and artificial inoculation by the endophytic fungus Apiognomonia errabunda of adult European beech trees. Environ Pollut 158:1043–1050PubMedCrossRefGoogle Scholar
  48. Osono T (2006) Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Can J Microbiol 52(8):701–716PubMedCrossRefGoogle Scholar
  49. Parker GG, Brown MJ (2000) Forest canopy stratification - is it useful? Am Nat 155(4):473–484PubMedCrossRefGoogle Scholar
  50. Pehl L, Butin H (1994) Endophytische Pilze in Blättern von Laubbäumen und ihre Beziehungen zu Blattgallen (Zoocecidien). Mitt Biol Bundesanst Land- Forstwirtsch 297:1–56Google Scholar
  51. Pereiro M Jr, Pereiro Ferreirós MM, De Hoog GS, Toribio J (2004) Cutaneous infection caused by Alternariae in patients receiving tacrolimus. Med Mycol 42:277–282Google Scholar
  52. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197CrossRefGoogle Scholar
  53. Promputtha I, Hyde KD, McKenzie EHC, Peberdy JF, Lumyong S (2010) Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers 41:89–99CrossRefGoogle Scholar
  54. Przybyl K (2002) Fungi associated with necrotic apical parts of Fraxinus excelsior shoots. For Pathol 32(6):387–394CrossRefGoogle Scholar
  55. Rensburg JCJ van, Lamprecht SC, Groenewald JZ, Castlebury LA, CrousPW (2006) Characterisation of Phomopsis spp. associated with die-backof rooibos (Aspalathus linearis) in South Africa. Stud Mycol 55:65–74Google Scholar
  56. Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330PubMedCrossRefGoogle Scholar
  57. Rodríguez J, Elissetche JP, Valenzuela S (2011) Tree endophytes and wood biodegradation. In: Pirttilä AM, Frank C (eds) Endophytes of forest trees: biology and applications. Forestry Series, Springer, Berlin, pp 81–93CrossRefGoogle Scholar
  58. Rohrschneider M (2007) Measurement of the canopy height and visualisation of its surface structure. In: Unterseher M, Morawetz W, Klotz S, Arndt E (eds) The Canopy of a Temperate Floodplain Forest - Results from five years of research at the Leipzig Canopy Crane. University of Leipzig, pp 18–20Google Scholar
  59. Schubert K, Ritschel A, Braun U (2003) A monograph of Fusicladium s. lat. (Hyphomycetes). Schlechtendalia 9:1–132Google Scholar
  60. Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, Hill CF,Zalar P, Hoog GS de, Crous PW (2007) Biodiversity in the Cladosporiumherbarum complex (Davidiellaceae, Capnodiales), with standardisation ofmethods for Cladosporium taxonomy and diagnostics. Stud Mycol58:105–156Google Scholar
  61. Schulz B, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25(1–3):213–227Google Scholar
  62. Seele C (2007) Tree species composition of the LAK investigation site. In: Unterseher M, Morawetz W, Klotz S, Arndt E (eds) The Canopy of a Temperate Floodplain Forest - Results from five years of research at the Leipzig Canopy Crane. University of Leipzig, pp 12–14Google Scholar
  63. Shaw DC (2004) Vertical organization of canopy biota. In: Lowman MD, Rinker HB (eds) Forest Canopies. 2nd edition, Elsevier, pp 73–101Google Scholar
  64. Sieber T, Hugentobler C (1987) Endophytic fungi in leaves and twigs of healthy and deseased beech trees (Fagus sylvatica L.). Eur J For Pathol 17(7):411–425CrossRefGoogle Scholar
  65. Simmons EG (2007) Alternaria: An Identification Manual, CBS Biodiversity Series 6. CBS, UtrechtGoogle Scholar
  66. Stamatakis A (2006) RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics 22(21):2688–2690PubMedCrossRefGoogle Scholar
  67. Stone JK (1987) Fine-structure of latent infections by Rhabdocline parkeri on Douglas-fir, with observations on uninfected epidermal cells. Can J Bot 66(1):45–54CrossRefGoogle Scholar
  68. Stone JK, Sherwood MA, Carroll GC (1996) Canopy microfungi: Function and diversity. Northwest Sci 70:37–45Google Scholar
  69. Suryanarayanan TS, Murali TS, Thirunavukkarasu N, Rajulu MBG, Venkatesan G, Sukumar R (2011) Endophytic fungal communities in woody perennials of three tropical forest types of the Western Ghats, southern India. Biodivers Conserv 20:913–928CrossRefGoogle Scholar
  70. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  71. Toti L, Viret O, Horat G, Petrini O (1993) Detection of the Endophyte Discula umbrinella In Buds and Twigs of Fagus-sylvatica. Eur J For Pathol 23(3):147–152CrossRefGoogle Scholar
  72. Ulrich W, Ollik M, Ugland KI (2010) A meta-analysis of species-abundance distributions. Oikos 119(7):1149–1155CrossRefGoogle Scholar
  73. Unterseher M (2011) Diversity of fungal endophytes in temperate forest trees. In: Pirttilä AM, Frank C (eds) Endophytes of forest trees: biology and applications. Forestry Series. Springer, Berlin, pp 31–46CrossRefGoogle Scholar
  74. Unterseher M, Schnittler M (2010) Species richness analysis and ITS rDNA phylogeny revealed the majority of cultivable foliar endophytes from beech (Fagus sylvatica). Fungal Ecol 3(4):366–378CrossRefGoogle Scholar
  75. Unterseher M, Tal O (2006) Influence of small scale conditions on the diversity of wood decay fungi in a temperate, mixed deciduous forest canopy. Mycol Res 110:169–178PubMedCrossRefGoogle Scholar
  76. Unterseher M, Reiher A, Finstermeier K, Otto P, Morawetz W (2007) Species richness and distribution patterns of leaf-inhabiting endophytic fungi in a temperate forest canopy. Mycol Prog 6(3):201–212CrossRefGoogle Scholar
  77. Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, Infante F, Castillo A, Arnold AE (2010) Fungal endophyte diversity in coffee plants from Colombia, Hawaii, Mexico and Puerto Rico. Fungal Ecol 3:122–138CrossRefGoogle Scholar
  78. Weber RWS, Anke H (2006) Effects of endophytes on colonisation by leaf surfacemicrobiota. In: Bailey MJ, Lilley AK, Timms-Wilson TM, Spencer-Phillips PTN (eds) Microbial Ecology of Aerial Plant Surfaces. CAB International, Wallingford, pp 209–222CrossRefGoogle Scholar
  79. White JJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols - a guide to methods and applications. Academic, San Diego, pp 315–322Google Scholar
  80. Wilson D (1996) Manipulation of infection levels of horizontally transmitted fungal endophytes in the field. Mycol Res 100:827–830CrossRefGoogle Scholar
  81. Wilson D, Carroll GC (1994) Infection studies of Discula quercina, an endophyte of Quercus garryana. Mycologia 86:635–647CrossRefGoogle Scholar
  82. Wilson D, Faeth SH (2001) Do fungal endophytes result in selection for leafminer ovipositional preference? Ecology 82(4):1097–1111CrossRefGoogle Scholar
  83. Wilson D, Barr ME, Faeth SH (1997) Ecology and description of a new species of Ophiognomonia endophytic in the leaves of Quercus emoryi. Mycologia 89(4):537–546CrossRefGoogle Scholar
  84. Wirsel SGR, Runge-Frobose C, Ahren DG, Kemen E, Oliver RP,Mendgen KW (2002) Four or more species of Cladosporiumsympatrically colonize Phragmites australis. Fungal Genet Biol 35:99–113Google Scholar
  85. Zalar P, Gostincar C, De Hoog GS, Ursic V, Sudhadham M, Gunde-Cimerman N (2008) Redefinition of Aureobasidium pullulans and itsvarieties. Stud Mycol 61:21–38Google Scholar

Copyright information

© German Mycological Society and Springer 2012

Authors and Affiliations

  • Almut Scholtysik
    • 1
  • Martin Unterseher
    • 2
  • Peter Otto
    • 3
  • Christian Wirth
    • 3
  1. 1.Institute for BiologyFreie Universität BerlinBerlinGermany
  2. 2.Institute of Botany and Landscape EcologyErnst-Moritz-Arndt-University GreifswaldGreifswaldGermany
  3. 3.Department of Special Botany and Functional Biodiversity ResearchUniversity of LeipzigLeipzigGermany

Personalised recommendations