Endophytic fungi in European aspen (Populus tremula) leaves - Diversity, detection, and a suggested correlation with herbivory resistance

Fungal Diversity

Volumn 41, Issue , 2010, Pages 17-28

  Albrectsen, Benedicte R ^a   Björkén, Lars ^a   Varad, Akkamahadevi ^a   Hagner, Åsa ^a,b   Wedin, Mats ^c   Karlsson, Jan ^a   Jansson, Stefan ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c SWEDISH MUSEUM OF NATURAL HISTORY   (Sweden)

Author keywords

Aureobasidium; Gene activity; Non clavicipitalean system; Phylogeny; Populus tremula; Primer design; Seasonality; Species richness

Indexed keywords

ASCOMYCOTA; AUREOBASIDIUM; AUREOBASIDIUM SP.; BASIDIOMYCOTA; DOTHIDEOMYCETES; EPICOCCUM; FUNGI; HYPOCREALES; PLEOSPORALES; POPULUS TREMULA; SORDARIOMYCETES; SPERMATOPHYTA; VENTURIA (FUNGUS);

EID: 79955839557     PISSN: 15602745     EISSN: None     Source Type: Journal    
DOI: 10.1007/s13225-009-0011-y     Document Type: Article

References (81)

1. Ahlholm J, Helander M, Elamo P, Saloniemi I, Neuvonen S, Hanhimäki S, Saikkonen K (2002) Micro-fungi and invertebrate herbivores on birch trees: fungal mediated plant-herbivore interactions or responses to host quality? Ecol Lett 5:648-655
2. Andersson A, Keskitalo J, Sjödin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Bhalerao R, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandberg G, Strauss S, Sundberg B, Uhlen M, Jansson S, Nilsson P (2004) A transcriptional timetable of autumn senescence. Genome Biol 5(4):R24
3. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges and frontiers. Fungal Biol Rev 21:51-66
4. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267-274
5. Arnold AE, Mejia LC, Kyllo D, Enith I, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649-15654
6. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185-206
7. Bailey JK, Deckert R, Schweitzer JA, Rehill BJ, Lindroth RL, Gehring C, Whitham TG (2005) Host plant genetics affect hidden ecological players, links among Populus, condensed tannins, and fungal endophyte infection. Can J Bot 83:356-361
8. Bazely DR, Vicari M, Emmerich S, Filip L, Lin D, Inman A (1997) Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish Islands of St. Kilda, Benbecula and Rum. J Appl Ecol 34:847-860
9. Bencheqroun SK, Baji M, Massart S, Labhilili M, El Jaafari S, Jijakli MH (2007) In vitro and in situ study of postharvest apple blue mold biocontrol by Aureobasidium pullulans: evidence for the involvement of competition for nutrients. Postharvest Biol Technol 46:128-135
10. Carroll G (1995) Forest endophytes-pattern and process. Can J Bot 73(S1):S1316-S1324
11. Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10-16
12. Curlevski N J A Xu ZH, Anderson IC, Cairney J W G (2010) Diversity of soil and rhizosphere fungi under Araucaria bidwillii (Bunya pine) at an Australian tropical montane rainforest site. Fungal Divers 40. doi:10.1007/s13225-009-0001-0.
13. Devarajan PT, Suryanarayanan TS (2006) Evidence for the role of phytophagous insects in dispersal of non-grass fungal endophytes. Fungal Divers 23:111-119
14. Duong LM, Jeewon R, Lumyong S, Hyde KD (2006) DGGE coupled with ribosomal DNA gene phylogenies reveal uncharacterized fungal phylotypes. Fungal Divers 23:121-138
15. Elamo P, Helander ML, Saloniemi I, Neuvonen S (1999) Birch family and environmental conditions affect endophytic fungi in leaves. Oecologia 118:151-156
16. Farris JS, Albert VA, Källersjö M, Lipscomb D, Kluge AG (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics 12:99-124
17. Faeth SH (2002) Are endophytic fungi defensice plant mutualists? Oikos 98:25-36
18. Faeth SH, Hammon KE (1997) Fungal endophytes in oak trees; long term patterns of abundance and associations with leafminers. Ecology 78:810-819
19. Ganley RJ, Brunsfeld SJ, Newcombe G (2004) A community of unknown, endophytic fungi in western white pine. Proc Natl Acad Sci USA 101:10107-10112
20. Gargas A, DePriest PT (1996) A nomenclature for fungal PCR primers with examples from intron-containing SSU rDNA. Mycologia 88:745-748
21. Giordano L, Gonthier P, Varese GC, Miserere L, Nicolotti G (2009) Mycobiota inhabiting sapwood of healthy and declining Scots pine (Pinus sylvestris L.) trees in the Alps. Fungal Divers 38:69-83
22. Gonthier P, Gennaro M, Nicolotti G (2006) Effects of water stress on the endophytic mycota of Quercus robur. Fungal Divers 21:69-80
23. Granath G, Vicari M, Bazely DR, Ball JP, Puentes A, Rakocevic T (2007) Variation in the abundance of fungal endophytes in fescue grasses along altitudinal and grazing gradients. Ecography 30:422-430
24. Grass Phylogeny Working Group (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373-457
25. Guo LD, Huang GR, Wang Y, He WH, Zheng WH, Hyde KD (2003) Molecular identification of white morphotype strains of endophytic fungi from Pinus tabulaeformis. Mycol Res 107:680-688
26. Hatcher MJ, Dick J T A Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9:1253-1271
27. Hibbett DS et al (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509-548
28. Hu HL, Jeewon R, Zhou DQ, Zhou TX, Hyde KD (2007) Phylogenetic diversity of endophytic Pestalotiopsis species in Pinus armandii and Ribes spp.: evidence from rDNA and β-tubulin gene phylogenies. Fungal Divers 24:1-22
29. Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61-75
30. Huang WY, Cai YZ, Surveswaran S, Hyde KD, Corke H, Sun M (2009) Molecular phylogenetic identification of endophytic fungi isolated from three Artemisia species. Fungal Divers 36:69-88
31. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163-173
32. Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945-953
33. Koh S, Hik DS (2007) Herbivory mediates grass-endophyte relationships. Ecology 88:2752-2757
34. Krohn K, Biele C, Drogies KH, Steingrover K, Aust HJ, Draeger S, Schulz B (2002) Fusidilactones, a new group of polycyclic lactones from an endophyte, Fusidium sp. Eur J Org Chem 14:2331-2336
35. Kumar D S S Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi from Tripterygium wilfordii. Fungal Divers 17:69-90
36. Lacap DC, Hyde KD, Liew E C Y (2003) An evaluation of the fungal 'morphotype' concept based on ribosomal DNA sequences. Fungal Divers 12:53-66
37. Lappalainen JH, Koricheva J, Helander ML, Haukioja E (1999) Densities of endophytic fungi and performance of leafminers (Lepidoptera, Eriocraniidae) on birch along a pollution gradient. Environ Pollut 104:99-105
38. Li WC, Zhou J, Guo SY, Guo LD (2007) Endophytic fungi associated with lichens in baihua mountain of Beijing, China. Fungal Divers 25:69-80
39. Luquez V, Hall D, Albrectsen BR, Karlsson J, Ingvarsson P, Jansson S (2008) Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genet Genomes 4:279-292
40. Mitchell AM, Strobel GA, Hess WM, Vargas PN, Ezra D (2008) Muscodor crispans, a novel endophyte from Ananas ananassoides in the Bolivian Amazon. Fungal Divers 31:37-43
41. Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289-1313
42. Osono T (2008) Endophytic and epiphytic phyllosphere fungi of Camelia japonica: sasonal and leaf age-dependent variations. Mycologia 100:387-391
43. Petrini O (1991) Endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Brock/Springer Series in Contemporary Bioscience, pp 179-196
44. Petrini O, Fisher PJ (1990) Occurrence of fungal endophytes in twigs of Salix fragilis and Quercus robur. Mycol Res 94:1077-1080
45. Preszler RW, Gaylord ES, Boecklen WJ (1996) Reduced parasitism of a leaf mining moth on trees with high infection frequencies of an endophytic fungus. Oecologia 108:159-166
46. Rudger JA, Clay K (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecol Lett 11:831-840
47. Rudger JA, Koslow JM, Clay K (2004) Endophytic fungi alter relationships between diversity and ecosystemproperties. Ecol Lett 7:42-51
48. Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones E B G (2008) Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oil palm, Elaeis guineensis, in Thailand. Fungal Divers 33:139-162
49. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols in the series methods in molecular biology. Humana Press, Totowa, pp 365-386, http://primer3.sourceforge.net
50. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67-74
51. Saikkonen K, Helander M, Ranta H, Neuvonen S, Virtanen T, Suomela L, Vuorinen P (1996) Endophyte mediated interactions between woody plants and insect herbivores. J Entomol Exp Appl 80:269-271
52. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Systemat 29:319-343
53. Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87-100
54. Santamaria O, Diez JJ (2005) Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain. Forest Pathol 35:95-104
55. Saona NM, Albrectsen BR, Ericson L, Bazely DR (2010) Environmental stresses mediate grass-endophyte interactions in a boreal archipelago. J Ecol. doi:10.1111/j.1365-2745.2009.01613.x
56. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661-686
57. Schulz B, Boyle C, Draeger S, Rmmert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996-1004
58. Schweitzer JA, Madritch MD, Bailey JK, LeRoy CJ, Fischer DG, Rehill BJ, Lindroth RL, Hagerman AE, Wooley SC, Hart SC, Whitham TG (2008) From genes to ecosystems: the genetic basis of condenced tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005-1020
59. Seena S, Wynberg N, Bärlocher F (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Divers 30:1-14
60. Segerman B, Jansson S, Karlsson J (2007) Characterization of genes with tissue-specific differential expression patterns in Populus. Tree Genet Genomes 3:351-362
61. Service RF (2006) The race for the 1000$ genome. Science 311:1544-1546
62. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75-89
63. Sjödin A, Bylesjö M, Skogström O, Eriksson D, Nilsson P, Rydén P, Jansson S, Karlsson J (2006) UPSC-BASE-Populus transcriptomics online. Plant J 48:806-817
64. Sjödin A, Wissel K, Bylesjö M, Trygg J, Jansson S (2008) Global expression profiling in leaves of free-growing aspen. Biomed Central Plant Biol 8:61
65. Skrzyñska M (2004) Studies on population frequency of insects and mites causing galls on the leaves of European aspen Populus tremula L. in southern Poland. J Pest Sci 77:119-122
66. Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260(5105):214-216
67. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Products 67:257-268
68. Suryanarayanan TS, Venkatesan G, Murali TS (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci 85:489-493
69. * and other methods), version 4.0b10. Sinauer Associates, Sunderland, Massachusetts, USA
70. Tao G, Liu ZY, Hyde KD, Lui XZ, Yu ZN (2008) Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers 33:101-122
71. Tejesvi MV, Kini KR, Prakash HS, ven Subbiah, Shetty HS (2007) Genetic diversity and antifungal activity of species of Pestalotiopsis isolated as endophytes from medicinal plants. Fungal Divers 24:37-54
72. Tejesvi MV, Tamhankar SA, Kini KR, Rao VS, Prakash HS (2009) Phylogenetic analysis of endophytic Pestalotiopsis species from ethnopharmaceutically important medicinal trees. Fungal Divers 38:167-183
73. Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan YN (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in populus. New Phytol 172:47-62
74. Tuskan GA et al (2006) The genome of black cottonwood, Populus tricocarpa (Torr. and Gray). Science 313:1596-1604
75. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, FischerM, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386-13391
76. Wang Y, Guo LD, Hyde KD (2005) Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in northeast China based on rDNA sequences. Fungal Divers 20:235-260
77. Webber JF (1981) A natural biological control of Dutch elm disease. Nature 292:449-451
78. Wedin M, Döring H, Gilenstam G (2006) Stictis s. lat. (Ostropales, Ascomycota) in northern Scandinavia, with a key and notes on morphological variation in relation to lifestyle. Mycol Res 110:773-789
79. White TJ, Bruns T, Lee S, Taylor JW (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, SanDiego, pp 315-322
80. Wilson D (1995) Endophyte-the evolution of a term, and clarification of its use and definition. Oikos 73:274-276
81. Wilson D, Carroll GC (1997) Avoidance of high-endophyte space by gall-forming insects. Ecology 78:2153-2163