Advertisement

Structure of Diversity in Dark Septate Endophytes: From Species to Genes

  • Christoph R. Grünig
  • Valentin Queloz
  • Thomas N. Sieber
Chapter
Part of the Forestry Sciences book series (FOSC, volume 80)

Abstract

Dark septate endophytes (DSE) are among the most abundant colonizers of plant roots. The form taxon DSE includes a broad range of fungal species that are only distantly related and the taxonomy of DSE has puzzled mycologists for years. In the following chapter we discuss the structure of diversity in dark septate endophytes. In the first part, we give an overview of the taxonomic placement of DSE and present a reference dataset of ITS sequences of well-characterized DSE taxa that can be used to classify DSE in future studies. The second part is dedicated to the diversity in the Phialocephala fortinii s.l. – Acephala applanata species complex (PAC), which includes some of the most frequent and widespread DSE. Diversity of PAC is discussed on various levels ranging from single root segments to continents and from communities to genes.

Keywords

Internal Transcribe Spacer Endophytic Fungus Dark Septate Endophyte Root Endophyte Hyaline Hypha 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

PAC

Phialocephala fortinii s.l. – Acephala applanata species complex

DSE

Dark septate endophytes

AMF

Arbuscular mycorrhizal fungi

BLAST

Basic local alignment search tool

MPV

Mollisia, Phaeomollisia and Vibrissea teleomorphs

ITS

Internal transcribed spacer

CSP

Cryptic species

MSR

Morphological species recognition

GCPSR

Genealogical concordance phylogenetic species recognition

RFLP

Restriction fragment length polymorphism

MLH

Multi-locus genotypes

AMOVA

Molecular variance analysis

Notes

Acknowledgements

We thank to Angelo Duo for sequencing the ITS regions of additional DSE isolates during the present study.

References

  1. Addy HD, Hambleton S, Currah RS (2000) Distribution and molecular characterization of the root endophyte Phialocephala fortinii along an environmental gradient in the boreal forest of Alberta. Mycol Res 104:1213–1221Google Scholar
  2. Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13Google Scholar
  3. Ahlich-Schlegel K (1997) Vorkommen und Charakterisierung von dunklen, septierten Hyphomyceten (DSH) in Gehölzwurzeln. PhD thesis, Swiss Federal Institute of Technology, Zürich, 170 pGoogle Scholar
  4. Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470Google Scholar
  5. Aveskamp MM, Verkley GJM, de Gruyter J et al (2009) DNA phylogeny reveals polyphyly of Phoma section Peyronellaea and multiple taxonomic novelties. Mycologia 101:363–382PubMedGoogle Scholar
  6. Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. van Stockum and Zoon, The HagueGoogle Scholar
  7. Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247PubMedGoogle Scholar
  8. Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalho GR (ed) Advances in molecular ecology, vol 309, NATO Science Series A. IOS Press, Amsterdam, pp 39–53Google Scholar
  9. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population size in n subpopulations by using a coalescent approach. Proc Natl Acad Sci 98:4563–4568PubMedGoogle Scholar
  10. Bell T, Ager D, Song JI et al (2005) Larger islands house more bacterial taxa. Science 308:1884–1884PubMedGoogle Scholar
  11. Bougoure DS, Cairney JWG (2005a) Assemblages of ericoid mycorrhizal and other root-associated fungi from Epacris pulchella (Ericaceae) as determined by culturing and direct DNA extraction from roots. Environ Microbiol 7:819–827PubMedGoogle Scholar
  12. Bougoure DS, Cairney JWG (2005b) Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environ Microbiol 7:1743–1754PubMedGoogle Scholar
  13. Bougoure JJ, Bougoure DS, Cairney JWG, Dearnaley JDW (2005) ITS-RFLP and sequence analysis of endophytes from Acianthus, Caladenia and Pterostylis (Orchidaceae) in southeastern Queensland. Mycol Res 109:452–460PubMedGoogle Scholar
  14. Brasier CM (1997) Fungal species in practice: identifying species units in fungi. In: Claridge M, Dawah H, Wilson M (eds) Species: the units of biodiversity. Chapmann & Hall, London, pp 135–170Google Scholar
  15. Brenn N, Menkis A, Grnig CR et al (2008) Community structure of Phialocephala fortinii s. lat. in European tree nurseries, and assessment of the potential of the seedlings as dissemination vehicles. Mycol Res 112:650–662PubMedGoogle Scholar
  16. Burnett J (2003) Fungal population and species. Oxford University Press, Oxford, 348 pGoogle Scholar
  17. Chambers SM, Liu G, Cairney JWG (2000) ITS rDNA sequence comparison of ericoid mycorrhizal endophytes from Woollsia pungens. Mycol Res 104:168–174Google Scholar
  18. Chaudhry MS, Rahman SU, Ismaiel MS et al (2009) Coexistence of arbuscular mycorrhizae and dark septate endophytic fungi in an undisturbed and a disturbed site of an arid ecosystem. Symbiosis 49:19–28Google Scholar
  19. Chen RS, Boeger JM, McDonald BA (1994) Genetic stability in a population of a plant pathogenic fungus over time. Mol Ecol 3:209–218Google Scholar
  20. Crous PW, Schubert K, Braun U et al (2007) Opportunistic, human-pathogenic species in the Herpotrichiellaceae are phenotypically similar to saprobic or phytopathogenic species in the Venturiaceae. Stud Mycol 58:185–234PubMedGoogle Scholar
  21. Currah RS, Sigler L, Hambleton S (1987) New records and new taxa of fungi from the mycorrhizae of terrestrial orchids of Alberta. Can J Bot 65:2473–2482Google Scholar
  22. Day MJ, Gibas CFC, Fujimura KE et al (2006) Monodictys arctica, a new hyphomycete from the roots of Saxifraga oppositifolia collected in the Canadian High Arctic. Mycotaxon 98:261–272Google Scholar
  23. de Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758PubMedGoogle Scholar
  24. Dettman JR, Jacobson DJ, Turner E et al (2003) Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution 57:2721–2741PubMedGoogle Scholar
  25. Dutech C, Enjalbert J, Fournier E et al (2007) Challenges of microsatellite isolation in fungi. Fung Genet Biol 44:933–949Google Scholar
  26. Eriksson OE, Hawksworth DL (2003) Saccharicola, a new genus for two Leptosphaeria species on sugar cane. Mycologia 95:426–433PubMedGoogle Scholar
  27. Excoffier L, Heckel G (2006) Computer programs for population genetics data analysis: a survival guide. Nat Rev Genet 7:745–758PubMedGoogle Scholar
  28. Excoffier L, Smouse P, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:343–359Google Scholar
  29. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  30. Fenchel T (2005) Cosmopolitan microbes and their ‘cryptic’ species. Aquat Microb Ecol 41:49–54Google Scholar
  31. Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784Google Scholar
  32. Fisher MC, Koenig GL, White TJ et al (2002) Molecular and phenotypic description of Coccidioides posadasii sp. nov., previously recognized as the non-California population of Coccidioides immitis. Mycologia 94:73–84PubMedGoogle Scholar
  33. Fuchs B, Haselwandter K (2004) Red list plants: colonization by arbuscular mycorrhizal fungi and dark septate endophytes. Mycorrhiza 14:277–281PubMedGoogle Scholar
  34. Geml J, Tulloss RE, Laursen GA et al (2008) Evidence for strong inter- and intracontinental phylogeographic structure in Amanita muscaria, a wind-dispersed ectomycorrhizal basidiomycete. Mol Phylogenet Evol 48:694–701PubMedGoogle Scholar
  35. Green JL, Bohannan BJM (2007) Biodiversity scaling relationships: are microorganisms fundamentally different? In: Storch D, Marquet PA, Brown JH (eds) Scaling biodiversity. Cambridge University Press, Cambridge, pp 129–149Google Scholar
  36. Green JL, Holmes AJ, Westoby M et al (2004) Spatial scaling of microbial eukaryote diversity. Nat 432:747–750Google Scholar
  37. Grünig CR, Sieber TN (2005) Molecular and phenotypic description of the widespread root symbiont Acephala applanata gen. et sp. nov., formerly known as dark septate endophyte type 1. Mycologia 97:628–640PubMedGoogle Scholar
  38. Grünig CR, Sieber TN, Rogers SO et al (2002a) Genetic variability among strains of Phialocephala fortinii and phylogenetic analysis of the genus Phialocephala based on rDNA ITS sequence comparisons. Can J Bot 80:1239–1249Google Scholar
  39. Grünig CR, Sieber TN, Rogers SO et al (2002b) Spatial distribution of dark septate endophytes in a confined forest plot. Mycol Res 106:832–840Google Scholar
  40. Grünig CR, Linde CC, Sieber TN et al (2003) Development of single-copy RFLP markers for population genetic studies of Phialocephala fortinii and closely related taxa. Mycol Res 107:1332–1341PubMedGoogle Scholar
  41. Grünig CR, McDonald BA, Sieber TN et al (2004) Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species. Fung Genet Biol 41:676–687Google Scholar
  42. Grünig CR, Duò A, Sieber TN (2006) Population genetic analysis of Phialocephala fortinii s.l. and Acephala applanata in two undisturbed forests in Switzerland and evidence for new cryptic species. Fung Genet Biol 43:410–421Google Scholar
  43. Grünig CR, Brunner PC, Duò A et al (2007) Suitability of methods for species recognition in the Phialocephala fortiniiAcephala applanata species complex using DNA analysis. Fung Genet Biol 44:773–788Google Scholar
  44. Grünig CR, Duò A, Sieber TN et al (2008a) Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s. l.-Acephala applanata species complex. Mycologia 100:47–67PubMedGoogle Scholar
  45. Grünig CR, Queloz V, Sieber TN et al (2008b) Dark septate endophytes (DSE) of the Phialocephala fortinii s.l. – Acephala applanata species complex in tree roots – classification, population biology and ecology. Botany 86:1355–1369Google Scholar
  46. Grünig CR, Queloz V, Duò A et al (2009) Phylogeny of Phaeomollisia piceae gen. sp. nov.: a dark-septate conifer-needle endophyte and its relationships to Phialocephala and Acephala. Mycol Res 113:207–221PubMedGoogle Scholar
  47. Grünwald NJ, Goodwin SB, Milgroom MG et al (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–746PubMedGoogle Scholar
  48. Halleen F, Schroers HJ, Groenewald JZ et al (2004) Novel species of Cylindrocarpon (Neonectria) and Campylocarpon gen. nov associated with black foot disease of grapevines (Vitis spp.). Stud Mycol 50:431–455Google Scholar
  49. Hambleton S, Sigler L (2005) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27Google Scholar
  50. Hambleton S, Huhtinen S, Currah R (1999) Hymenoscyphus ericae: a new record from western Canada. Mycol Res 103:1391–1397Google Scholar
  51. Harrington T, Mcnew D (2003) Phylogenetic analysis places the Phialophora-like anamorph genus Cadophora in the Helotiales. Mycotaxon 87:141–151Google Scholar
  52. Hartl DL, Clark AG (1989) Principles of population genetics, 2nd edn. Sinauer Associates, Sunderland, 682 pGoogle Scholar
  53. Holsinger KE, Weir BS (2009) Genetics in geographically structured populations: defining, estimating and interpreting FST. Nat Rev Genet 10:639–650PubMedGoogle Scholar
  54. Hurlbert SH (1971) Nonconcept of species diversity – critique and alternative parameters. Ecology 52:577–586Google Scholar
  55. Jacobson DJ, Dettman JR, Adams RI et al (2006) New findings of Neurospora in Europe and comparisons of diversity in temperate climates on continental scales. Mycologia 98:550–559PubMedGoogle Scholar
  56. James TY, Porter D, Hamrick JL et al (1999) Evidence for limited intercontinental gene flow in the cosmopolitan mushroom, Schizophyllum commune. Evolution 53:1665–1677Google Scholar
  57. Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429PubMedGoogle Scholar
  58. Kai W, Zhao ZW (2006) Occurrence of arbuscular mycorrhizas and dark septate endophytes in hydrophytes from lakes and streams in southwest China. Int Rev Hydrobiol 91:29–37Google Scholar
  59. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543Google Scholar
  60. Kauserud H, Lie M, Stensrud O et al (2005) Molecular characterization of airborne fungal spores in boreal forests of contrasting human disturbance. Mycologia 97:1215–1224PubMedGoogle Scholar
  61. Khidir HH, Eudy DM, Porras-Alfaro A et al (2010) A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J Arid Environ 74:35–42Google Scholar
  62. Kirk PM, Cannon PF, David JC et al (eds) (2001) Dictionary of the fungi, 9th edn. CAB International, Oxon, 655 pGoogle Scholar
  63. Koufopanou V, Burt A, Taylor JW (1997) Concordance of gene genealogies reveals reproductive isolation in the pathogenic fungus Coccidioides immitis. Proc Natl Acad Sci 94:5478–5482PubMedGoogle Scholar
  64. Koufopanou V, Burt A, Szaro T et al (2001) Gene genealogies, cryptic species, and molecular evolution in the human pathogen Coccidioides immitis and relatives (Ascomycota, Onygenales). Mol Biol Evol 18:1246–1258PubMedGoogle Scholar
  65. Kowalski T, Bartnik C (1995) Cryptosploriopsis radicicola sp. nov from roots of Quercus robur. Mycol Res 99:663–666Google Scholar
  66. Kowalski T, Kehr RD (1995) Two new species of Phialocephala occurring on Picea and Alnus. Can J Bot 73:26–32Google Scholar
  67. Kowalski T, Halmschlager E, Schrader K (1998) Cryptosporiopsis melanigena sp. nov., a root-inhabiting fungus of Quercus robur and Q. petraea. Mycol Res 102:347–354Google Scholar
  68. Lehnert M, Kottke I, Setaro S et al (2009) Mycorrhizal associations in ferns from southern Ecuador. Am Fern J 99:292–306Google Scholar
  69. Liang C, Xiao Y, Zhao Z (2007) Arbuscular mycorrhiza and dark septate endophytes in an abandoned lead-zinc mine in Huize, Yunnan, China. Chin J Appl Environ Biol 13:811–817Google Scholar
  70. Likar M, Regvar M, Mandic-Mulec I et al (2009) Diversity and seasonal variations of mycorrhiza and rhizosphere bacteria in three common plant species at the Slovenian Ljubljana Marsh. Biol Fertil Soils 45:573–583Google Scholar
  71. Linde CC, Zhan J, McDonald BA (2002) Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92:946–955PubMedGoogle Scholar
  72. Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821PubMedGoogle Scholar
  73. Manici LM, Caputo F (2009) Fungal community diversity and soil health in intensive potato cropping systems of the east Po valley, northern Italy. Ann Appl Biol 155:245–258Google Scholar
  74. Martiny JBH, Bohannan BJM, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112PubMedGoogle Scholar
  75. McDonald BA (1997) The population genetics of fungi: tools and techniques. Phytopathology 87:448–453PubMedGoogle Scholar
  76. McGill BJ, Etienne RS, Gray JS et al (2007) Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol Lett 10:995–1015PubMedGoogle Scholar
  77. Menkis A (2005) Root associated fungi of conifer seedlings and their role in afforestation of agricultural land. PhD thesis, Swedish University of Agricultural Sciences, UppsalaGoogle Scholar
  78. Menkis A, Allmer J, Vasiliauskas R et al (2004) Ecology and molecular characterization of dark septate fungi from roots, living stems, coarse and fine woody debris. Mycol Res 108:965–973PubMedGoogle Scholar
  79. Midgley DJ, Chambers SM, Cairney JWG (2002) Spatial distribution of fungal endophyte genotypes in a Woollsia pungens (Ericaceae) root system. Aust J Bot 50:559–565Google Scholar
  80. Midgley DJ, Chambers SM, Cairney JWG (2004) Distribution of ericoid mycorrhizal endophytes and root- associated fungi in neighbouring Ericaceae plants in the field. Plant Soil 259:137–151Google Scholar
  81. Milgroom MG (1996) Recombination and the multilocus structure of fungal populations. Annu Rev Phytopathol 34:457–477PubMedGoogle Scholar
  82. Möller C, Dreyfuss MM (1996) Microfungi from Antarctic lichens, mosses and vascular plants. Mycologia 88:922–933Google Scholar
  83. Münzenberger B, Bubner B, Wöllecke J et al (2009) The ectomycorrhizal morphotype Pinirhiza sclerotia is formed by Acephala macrosclerotia sp. nov., a close relative of Phialocephala fortinii. Mycorrhiza 19:481–492PubMedGoogle Scholar
  84. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci 70:3321–3323PubMedGoogle Scholar
  85. Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20Google Scholar
  86. O’Donnell K, Ward TJ, Geiser DM et al (2004) Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fung Genet Biol 41:600–623Google Scholar
  87. O’Malley MA (2007) The nineteenth century roots of ‘everything is everywhere’. Nat Rev Microbiol 5:647–651PubMedGoogle Scholar
  88. Peay KG, Kennedy PG, Bruns TD (2008) Fungal community ecology: a hybrid beast with a molecular master. Bioscience 58:799–810Google Scholar
  89. Petersen RH, Hughes KW (1999) Species and speciation in mushrooms. Bioscience 49:440–452Google Scholar
  90. Pielou EC (1977) Association between pairs of species I: individuals in discrete habitable units. In: Mathematical ecology. Wiley, New York, pp 203–239Google Scholar
  91. Piercey MM, Graham SW, Currah RS (2004) Patterns of genetic variation in Phialocephala fortinii across a broad latitudinal transect in Canada. Mycol Res 108:955–964PubMedGoogle Scholar
  92. Pringle A, Baker DM, Platt JL et al (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–1899PubMedGoogle Scholar
  93. Queloz V (2008) La face cachée du Creux du Van: presence des endophytes racinaires Phialocephala fortinii s.l. et Acephala applanata sur le pergélisole du Creux du Van. Actes de la société jurassienne d’émulation 2007:107–126Google Scholar
  94. Queloz V, Grünig CR, Sieber TN et al (2005) Monitoring the spatial and temporal dynamics of a community of the tree-root endophyte Phialocephala fortinii s.l. New Phytol 168:651–660PubMedGoogle Scholar
  95. Queloz V, Duo A, Sieber TN et al (2010) Microsatellite size homoplasies and null alleles do not affect species diagnosis and population genetic analysis in a fungal species complex. Mol Ecol Res 10:348–367Google Scholar
  96. Queloz V, Sieber TN, Holdenrieder O et al (2011) No biogeographical pattern for a root-associated fungal species complex. Global Ecol Biogeogr 20:160–169. doi:DOI: 10.1111/j.1466-8238.2010.00589.xGoogle Scholar
  97. Radisek S, Leskosek G, Jakse J et al (2009) Occurrence of Cercospora cantuariensis on hop in Austria and Slovenia. Plant Path 58:400–400Google Scholar
  98. Read DJ (1974) Pezizella ericae sp. nov, perfect state of a typical mycorrhizal endophyte of Ericaceae. Trans Brit Mycol Soc 63:381Google Scholar
  99. Read DJ, Haselwandter K (1981) Observations on the mycorrhizal status of some alpine plant communities. New Phytol 88:341–345Google Scholar
  100. Rousset F (2008) GENEPOP ’ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106Google Scholar
  101. Ruibal C, Platas G, Bills GF (2008) High diversity and morphological convergence among melanised fungi from rock formations in the Central Mountain System of Spain. Persoonia 21:93–110PubMedGoogle Scholar
  102. Saleh AA, Leslie JE (2004) Cephalosporium maydis is a distinct species in the Gaeumannomyces harpophora species complex. Mycologia 96:1294–1305PubMedGoogle Scholar
  103. Sánchez Márquez S, Bills GF et al (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fung Div 33:87–100Google Scholar
  104. Sánchez Márquez S, Bills GF, Domínguez Acuña L et al (2010) Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fung Div 41:115–123Google Scholar
  105. Schol-Schwarz MB (1970) Revision of the genus Phialophora (Moniliales). Persoonia 6:59–94Google Scholar
  106. Schroers HJ, Zerjav M, Munda A et al (2008) Cylindrocarpon pauciseptatum sp. nov., with notes on Cylindrocarpon species with wide, predominantly 3-septate macroconidia. Mycol Res 112:82–92PubMedGoogle Scholar
  107. Sieber TN (2002) Fungal root endophytes. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker, New York/Basel, pp 887–917Google Scholar
  108. Sieber TN, Grünig CR (2006) Biodiversity of fungal root-endophyte communities and populations in particular of the dark septate endophyte Phialocephala fortinii. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Soil biology series. Springer, Berlin, pp 107–132Google Scholar
  109. Sigler L, Allan T, Lim SR et al (2005) Two new Cryptosporiopsis species from roots of ericaceous hosts in western North America. Stud Mycol 53:53–62Google Scholar
  110. Stoddart JA, Taylor JF (1988) Genotypic diversity – estimation and prediction in samples. Genetics 118:705–711PubMedGoogle Scholar
  111. Stoyke G, Currah RS (1991) Endophytic fungi from the mycorrhizae of alpine ericoid plants. Can J Bot 69:347–352Google Scholar
  112. Stukenbrock EH, Banke S, McDonald BA (2006) Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Mol Ecol 15:2895–2904PubMedGoogle Scholar
  113. Sunnucks P (2000) Efficient genetic markers for population biology. Tree 15:199–203PubMedGoogle Scholar
  114. Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504PubMedGoogle Scholar
  115. Tanaka K, Hosoya T (2008) Lophiostoma sagittiforme sp nov., a new ascomycete (Pleosporales, Dothideomycetes) from Island Yakushima in Japan. Sydowia 60:131–145Google Scholar
  116. Taylor JW, Jacobson DJ, Kroken S et al (2000) Phylogenetic species recognition and species concepts in fungi. Fung Genet Biol 31:21–32Google Scholar
  117. Taylor JW, Turner E, Townsend JP et al (2006) Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Philos Trans R Soc B Biol Sci 361:1947–1963Google Scholar
  118. Templeton AR (1981) Mechanisms of speciation – a population genetic approach. Annu Rev Ecol Syst 12:23–48Google Scholar
  119. Verkley G, Zijlstra J, Summerbell R et al (2003) Phylogeny and taxonomy of root-inhabiting Cryptosporiopsis species, and C. rhizophila sp nov., a fungus inhabiting roots of several Ericaceae. Mycol Res 107:689–698PubMedGoogle Scholar
  120. Wang CJK, Wilcox HE (1985) New species of ectendomycorrhizal and pseudomycorrhizal fungi: Phialophora finlandia, Chloridium paucisporum, and Phialocephala fortinii. Mycologia 77:951–958Google Scholar
  121. Wang Z, Johnston PR, Takamatsu S et al (2006) Toward a phylogenetic classification of the Leotiomycetes based on rDNA data. Mycologia 98:1065–1075PubMedGoogle Scholar
  122. Wang W, McGhee D, Gibas CFC et al (2009) Phialocephala urceolata, sp. nov., from a commercial, water-soluble heparin solution. Mycologia 101:136–141PubMedGoogle Scholar
  123. Weishampel PA, Bedford BL (2006) Wetland dicots and monocots differ in colonization by arbuscular mycorrhizal fungi and dark septate endophytes. Mycorrhiza 16:495–502PubMedGoogle Scholar
  124. Weising K, Nybom H, Wolff K et al (1995) DNA fingerprinting in plants and fungi. CRC, Boca Raton, 322 pGoogle Scholar
  125. Wilberforce EM, Boddy L, Griffiths R et al (2003) Agricultural management affects communities of culturable root-endophytic fungi in temperate grasslands. Soil Biol Biochem 35:1143–1154Google Scholar
  126. Wilson BJ, Addy HD, Tsuneda A et al (2004) Phialocephala sphaeroides sp nov., a new species among the dark septate endophytes from a boreal wetland in Canada. Can J Bot 82:607–617Google Scholar
  127. Wu L-q, Lv Y-l, Meng Z-x et al (2010) The promoting role of an isolate of dark-septate fungus on its host plant Saussurea involucrata Kar. et Kir. Mycorrhiza 20:127–135PubMedGoogle Scholar
  128. Yang J, Smith HG, Sherratt TN et al (2010) Is there a size limit for cosmopolitan distribution in free-living microorganisms? Biogeographical analysis testate Amoebae polar areas. Microb Ecol 59:635–645PubMedGoogle Scholar
  129. Yeh FC, Yang R, Boyle T (1999) POPGENE version 1.31. Microsoft window-based freeware for population genetic AnalysisGoogle Scholar
  130. Yu T, Nassuth A, Peterson RL (2001) Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Can J Microbiol 47:741–753PubMedGoogle Scholar
  131. Yuan Z-l, Zhang C-l, Lin F-c et al (2010) Identity, diversity, and molecular phylogeny of the endophytic mycobiota in the roots of rare wild rice (Oryza granulate) from a nature reserve in Yunnan, China. Appl Environ Microb 76:1642–1652Google Scholar
  132. Zhan J, Pettway R, McDonald B (2003) The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fung Genet Biol 38:286–297Google Scholar
  133. Zubek S, Blaszkowski J, Delimat A et al (2009) Arbuscular mycorrhizal and dark septate endophyte colonization along altitudinal gradients in the Tatra Mountains. Arct Antarct Alp Res 41:272–279Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Christoph R. Grünig
    • 1
  • Valentin Queloz
    • 1
  • Thomas N. Sieber
    • 1
  1. 1.Forest Pathology and DendrologyETH Zürich, Institute of Integrative Biology (IBZ)ZürichSwitzerland

Personalised recommendations