Skip to main content

Advertisement

Log in

Leaf-inhabiting endophytic fungi of European Beech (Fagus sylvatica L.) co-occur in leaf litter but are rare on decaying wood of the same host

  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

Many microfungi are able to live in living plant tissues. In contrast to plant pathogens and parasites the so-called endophytic fungi do not cause obvious disease symptoms in their hosts. Nevertheless, they constitute an ubiquitous active component in direct and multitrophic interactions. The present study was conducted to assess the level of overlap of cultivable microfungi in living and decaying tissues of European Beech (Fagus sylvatica L.) from a forest stand in North-Eastern Germany. The focus lay on the hypothesized fall-spring relationship of leaf-inhabiting forest endophytes, which means that endophytes from autumn leaves persist as saprobes in litter or dead wood, sporulate and re-invade living leaves in spring. Fungal cultures were isolated from living leaves, leaf litter and dead wood still attached to the tree by dilution-to-extinction cultivation in the years 2007–2010. Analyses of species identity, species richness and species composition were based on microscopic identification and of sequencing the fungal DNA ‘barcode’ ITS (internal transcribed spacer). Species richness of litter-inhabiting microfungi equaled that of wood-inhabiting fungi and exceeded that of leaf endophytes. The most distinctive species assemblage was observed on wood, fungal species composition in living leaves and leaf litter were also significantly different from each other. On the other hand a considerable compositional and phylogenetic overlap between leaf and litter fungi was revealed with phylogenetics, cluster analysis and non-metric multidimensional scaling. The taxa accounting most to the similarity between living and decaying leaves belonged to Capnodiales, Xylariales, Diaporthales and Pleosporales. Finally, data from cultivated leaf-inhabiting beech endophytes were compared with a fungal 454 sequence data set from beech phyllosphere. This analysis allowed the partition of species lists into active fungal endophytes, fungal “epiphytes” and dormant fungal propagules.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aly AH, Debbab A, Proksch P (2011) Fifty years of drug discovery from fungi. Fungal Divers 50:3–19

    Article  Google Scholar 

  • Amend A, Seifert K, Bruns T (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565

    Article  PubMed  CAS  Google Scholar 

  • Andrews JH, Kinkel LL, Berbee FM et al (1987) Fungi, leaves, and the theory of island biogeography. Microb Ecol 14:277–290

    Article  Google Scholar 

  • Bahnweg G, Heller W, Stich S et al (2005) Beech leaf colonization by the endophyte Apiognomonia errabunda dramatically depends on light exposure and climatic conditions. Plant Biol 7:659–669

    Article  PubMed  CAS  Google Scholar 

  • Bailey JK, Deckert R, Schweitzer JA et al (2005) Host plant genetics affect hidden ecological players: links among, condensed tannins, and fungal endophyte infection. Can J Bot 83:356–361

    Article  Google Scholar 

  • Bayman P (2006) Diversity, scale and variation of endophytic fungi in leaves of tropical plants. In: Bailey MJ, Lilley AK, Timms-Wilson TM et al (eds) Microbial ecology of aerial plant surfaces. CABI International, Cambridge, pp 37–50

    Chapter  Google Scholar 

  • Bills GF, González-Menéndez V, Martín J et al (2012) Hypoxylon pulicicidum sp. nov. (Ascomycota, Xylariales), a pantropical insecticide-producing endophyte. PLoS One 7:e46687

    Article  PubMed  CAS  Google Scholar 

  • Boddy L (1992) Development and function of fungal communities in decomposing wood. In: Carroll GC, Wicklow DT (eds) The fungal community, its organization and role in the ecosystem, 2nd edn. Marcel Dekker, New York, pp 749–782

    Google Scholar 

  • Boddy L, Rayner ADM (1983) Mycelial interactions, morphogenesis and ecology of Phlebia radiata and P. rufa from oak. Trans Br Mycol Soc 80:437–448

    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 

  • Buée M, Reich M, Murat C et al (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    Article  PubMed  Google Scholar 

  • Cabral A, Groenewald JZ, Rego C et al (2012) Cylindrocarpon root rot: multi-gene analysis reveals novel species within the Ilyonectria radicicola species complex. Mycol Prog 11:655–688

    Article  Google Scholar 

  • Carroll G, Petrini O (1983) Patterns of substrate utilization by some fungal endophytes from coniferous foliage. Mycologia 75:53

    Article  Google Scholar 

  • Chaverri P, Salgado C, Hirooka Y et al (2011) Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon-like anamorphs. Stud Mycol 68:57–78

    Article  PubMed  CAS  Google Scholar 

  • Coddington J, Agnarsson I, Miller J et al (2009) Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. J Anim Ecol 78:573–584

    Article  PubMed  Google Scholar 

  • Collado J, Platas G, Paulus B et al (2007) High-throughput culturing of fungi from plant litter by a dilution-to-extinction technique. FEMS Microbiol Ecol 60:521–533

    Article  PubMed  CAS  Google Scholar 

  • Colwell R, Coddington J (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118

    Article  PubMed  CAS  Google Scholar 

  • Cordier T, Robin C, Capdevielle X et al (2012a) Spatial variability of phyllosphere fungal assemblages: genetic distance predominates over geographic distance in a European beech stand (Fagus sylvatica). Fungal Ecol 5:509–520

    Article  Google Scholar 

  • Cordier T, Robin C, Capdevielle X et al (2012b) The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica) varies significantly along an elevation gradient. New Phytol 196:510–519

    Article  PubMed  Google Scholar 

  • Davis E, Franklin J, Shaw A et al (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 90:1661–1667

    Article  PubMed  Google Scholar 

  • de Hoog GS, van den Ende AHG (1998) Molecular diagnostics of clinical strains of filamentous basidiomycetes. Mycoses 41:183–189

    Article  PubMed  Google Scholar 

  • Debbab A, Aly AH, Proksch P (2012) Endophytes and associated marine derived fungi–ecological and chemical perspectives. Fungal Divers 57:45–83

    Article  Google Scholar 

  • Faeth SH, Saari S (2012) Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions. Fungal Ecol 5:364–371

    Article  Google Scholar 

  • Fell JW, Boekhout T, Fonseca A et al (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1371

    Article  PubMed  CAS  Google Scholar 

  • Flessa F, Peršoh D, Rambold G (2012) Annuality of Central European deciduous tree leaves delimits community development of epifoliar pigmented fungi. Fungal Ecol 5:554–561

    Article  Google Scholar 

  • Fröhlich-Nowoisky J, Pickersgill D, Despres V et al (2009) High diversity of fungi in air particulate matter. Proc Natl Acad Sci U S A 106:12814–12819

    Article  PubMed  Google Scholar 

  • Fukasawa Y, Osono T, Takeda H (2009) Effects of attack of saprobic fungi on twig litter decomposition by endophytic fungi. Ecol Res 24:1067–1073

    Article  Google Scholar 

  • Gonda S, Kiss A, Emri T et al (2013) Filamentous fungi from Plantago lanceolata L. leaves: contribution to the pattern and stability of bioactive metabolites. Phytochemistry 86:127–136

    Article  PubMed  CAS  Google Scholar 

  • Gonthier P, Gennaro M, Nicolotti G (2006) Effects of water stress on the endophytic mycota of Quercus robur. Fungal Divers 21:69–80

    Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Gotz M, Nirenberg H, Krause S et al (2006) Fungal endophytes in potato roots studied by traditional isolation and cultivation-independent DNA-based methods. FEMS Microbiol Ecol 58:404–413

    Article  PubMed  Google Scholar 

  • Govinda R, Meenavalli B, Thirunavukkarasu N, Suryanarayanan TS et al (2011) Chitinolytic enzymes from endophytic fungi. Fungal Divers 47:43–53

    Article  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M et al (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10

    Article  Google Scholar 

  • Heilmann-Clausen J, Christensen M (2004) Does size matter? on the importance of various dead wood fractions for fungal diversity in Danish beech forests. Forest Ecol Manag 201:105–117

    Article  Google Scholar 

  • Hofstetter V, Buyck B, Croll D et al (2012) What if esca disease of grapevine were not a fungal disease? Fungal Divers 54:51–67

    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 

  • Jumpponen A, Jones K (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298

    Article  PubMed  CAS  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW et al (2008) Ainsworth & Brisby’s dictionary of the fungi. CABI Publishing, UK

    Google Scholar 

  • Korkama-Rajala T, Muller M, Pennanen T (2008) Decomposition and fungi of needle litter from slow- and fast-growing Norway spruce (Picea abies) clones. Microb Ecol 56:76–89

    Article  PubMed  Google Scholar 

  • Lacap DC, Hyde KD, Liew ECY (2003) An evaluation of the fungal ‘morphotype’ concept based on ribosomal DNA sequences. Fungal Divers 12:53–66

    Google Scholar 

  • Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis Version 2.75. http://mesquiteproject.org (last assessed October 2012)

  • Nilsson RH, Veldre V, Hartmann M et al (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 3:284–287

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest [computer program]. Version 2.1. Uppsala: Evolutionary Biology Centre, Uppsala University, by the author

  • Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. Available at http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf (last assessed October 2012)

  • Öpik M, Metsis M, Daniell T et al (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–437

    Article  PubMed  Google Scholar 

  • 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 52:701–716

    Article  PubMed  CAS  Google Scholar 

  • Osono T, Takeda H (1999) Decomposing ability of interior and surface fungal colonizers of beech leaves with reference to lignin decomposition. Eur J Soil Biol 35:51–56

    Article  Google Scholar 

  • Parfitt D, Hunt J, Dockrell D et al (2010) Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol 3:338–346

    Article  Google Scholar 

  • Paulus B, Gadek P, Hyde KD (2003) Estimation of microfungal diversity in tropical rainforest leaf litter using particle filtration: the effects of leaf storage and surface treatment. Mycol Res 107:748–756

    Article  PubMed  Google Scholar 

  • Peay K, Bruns T, Kennedy P et al (2007) A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480

    Article  PubMed  Google Scholar 

  • Peršoh D (2013) Factors shaping community structure of endophytic fungi–evidence from the Pinus-Viscum-system. Fungal Diversity: manuscript ID: FUDI-S-12-00361

  • Peršoh D, Melcher M, Flessa F et al (2010) First fungal community analyses of endophytic ascomycetes associated with Viscum album ssp. austriacum and its host Pinus sylvestris. Fungal Biol 114:585–596

    Article  PubMed  Google Scholar 

  • Peršoh D, Segert J, Zigan A et al (2013) Fungal community composition shifts along a leaf degradation gradient in a European beech forest. Plant Soil 362:175–186

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  PubMed  CAS  Google Scholar 

  • Promputtha I, Lumyong S, Dhanasekaran V et al (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53:579–590

    Article  PubMed  Google Scholar 

  • Promputtha I, Hyde KD, Mckenzie EHC et al (2010) Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers 41:89–99

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. Available from http://www.R-project.org (last assessed October 2012)

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

    Article  PubMed  CAS  Google Scholar 

  • Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113

    Article  Google Scholar 

  • Santamaria J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microb Ecol 50:1–8

    Article  PubMed  Google Scholar 

  • Schnittler M, Tesmer J (2008) A habitat colonisation model for spore-dispersed organisms: does it work with eumycetozoans? Mycol Res 112:697–707

    Article  PubMed  Google Scholar 

  • Schulz B, Wanke U, Draeger S et al (1993) Endophytes from herbaceous plants and shrubs: effectiveness of surface sterilization methods. Mycol Res 97:1447–1450

    Article  Google Scholar 

  • Seifert K, Morgan-Jones G, Gams W, et al. (2011) The genera of hyphomycetes. CBS Biodiversity Series 9. 997 pp, CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands

  • Sieber T, Hugentobler C (1987) Endophytic fungi in leaves and twigs of healthy and diseased beech trees (Fagus sylvatica L.). Eur J Forest Pathol 17:411–425

    Article  Google Scholar 

  • Sun Y, Wang Q, Lu X et al (2011) Endophytic fungal community in stems and leaves of plants from desert areas in China. Mycol Prog 11:781–790

    Article  Google Scholar 

  • Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB et al (2012) Fungal endophytes: an untapped source of biocatalysts. Fungal Divers 54:19–30

    Article  Google Scholar 

  • Tedersoo L, Nilsson R, Abarenkov K et al (2010) 454 pyrosequencing and sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188:291–301

    Article  PubMed  CAS  Google Scholar 

  • Ulrich W, Ollik M, Ugland KI (2010) A meta-analysis of species-abundance distributions. Oikos 119:1149–1155

    Article  Google Scholar 

  • Unterseher M (2011) Diversity of fungal endophytes in temperate forest trees. In: Pirttilä AM, Frank AC (eds) Endophytes of forest trees: biology and applications. Springer Netherlands, Dordrecht, pp 31–46

    Chapter  Google Scholar 

  • Unterseher M, Schnittler M (2009) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)–different cultivation techniques influence fungal biodiversity assessment. Mycol Res 113:645–654

    Article  PubMed  Google Scholar 

  • 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 3:366–378

    Article  Google Scholar 

  • 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 110:169–178

    Article  PubMed  Google Scholar 

  • Unterseher M, Jumpponen A, Opik M et al (2011) Species abundance distributions and richness estimations in fungal metagenomics–lessons learned from community ecology. Mol Ecol 20:275–285

    Article  PubMed  Google Scholar 

  • Unterseher M, Petzold A, Schnittler M (2012) Xerotolerant foliar endophytic fungi of Populus euphratica from the Tarim River basin, Central China are conspecific to endophytic ITS phylotypes of Populus tremula from temperate Europe. Fungal Divers 54:133–142

    Article  Google Scholar 

  • Verkley GJM, Crous PW, Groenewald JZE et al (2004) Mycosphaerella punctiformis revisited: morphology, phylogeny, and epitypification of the type species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycol Res 108:1271–1282

    Article  PubMed  CAS  Google Scholar 

  • Weber RWS, Anke H (2006) Effects of endophytes on colonisation by leaf surface microbiota. In: Bailey MJ, Lilley AK, Timms-Wilson TM et al (eds) Microbial ecology of aerial plant surfaces. CABI International, Cambridge, pp 209–222

    Chapter  Google Scholar 

  • Weiß M, Sykorova Z, Garnica S et al (2011) Sebacinales everywhere: previously overlooked ubiquituous fungal endophytes. PLoS One 6:e16793

    Article  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S et al (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ et al (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Yurkov A, Kemler M, Begerow D (2011) Species accumulation curves and incidence-based species richness estimators to appraise the diversity of cultivable yeasts from beech forest soils. PLoS One 6:e23671

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Song Y, Tan R (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the SYNTHESYS network (grant NL-TAF- 4477) that permitted a 3-week stay of MU at CBS Fungal Biodiversity Centre, Utrecht, in December 2008. MU also thanks Pedro Crous, Gerard Verkley, Geert van Haalem and further personnel from the CBS for the provision of infrastructure and expertise (including species identification) during that time. The two Diploma students Tina Jatzkowski and Hauke Duhm and the lab technician Anja Klahr (all Greifswald) is thanked for their great assistance. Two reviewers is thanked for valuable comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Unterseher.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLS 223 kb)

ESM 2

(TXT 11 kb)

ESM 3

(TXT 4 kb)

ESM 4

(TXT 0 kb)

ESM 5

(TXT 0 kb)

ESM 6

(TXT 1 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Unterseher, M., Peršoh, D. & Schnittler, M. Leaf-inhabiting endophytic fungi of European Beech (Fagus sylvatica L.) co-occur in leaf litter but are rare on decaying wood of the same host. Fungal Diversity 60, 43–54 (2013). https://doi.org/10.1007/s13225-013-0222-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-013-0222-0

Keywords

Navigation