Fungal Diversity

, Volume 41, Issue 1, pp 29–40 | Cite as

Diversity and significance of fungal endophytes from living stems of naturalized trees from Argentina

  • A. de Errasti
  • C. C. Carmarán
  • M. Victoria Novas


Fungal endophytes inhabit healthy tissues of all terrestrial taxa studied to date; however, fungi associated with woody tissue have been frequently overlooked. Here, we examined endophytes associated with healthy living stems of tree species exotic to Argentina (Broussonetia papyrifera, Celtis occidentalis and Ligustrum lucidum) in a natural reserve. To achieve this objective, fungi were induced to develop within the wood by drying sections of branches. For comparison purposes, a study of the organisms present on superficial and inner bark was carried out. Fifty-seven strains belonging to 12 different taxa, dominated by the anamorphic states of ascomycetes, were obtained from the 180 cultured chips. Coprinellus micaceus, Lecythophora hoffmannii and Rhizopus microsporus are cited for the first time as endophytes. Only two taxa appeared on more than one tree species. Assemblages of fungi obtained from each tree species were different and the fungal endophytes isolated were very different from those previously recorded for leaves of the same hosts in the same area. Thus, it is probable that the endophytes exhibit host- and tissue-specificity. Considering three main factors: 1. the invasive nature of two of the selected hosts, 2. the evaluation of woody tissue and 3. the taxonomic identity of the fungal isolations, hypotheses concerning ecological implications are here discussed. In this sense, Broussonetia papyrifera and Ligustrum lucidum could be considered as sources of potential inoculum for native plants, especially in protected areas, and the high diversity of fungal species living within the tissues of the hosts studied suggests their potential as important fungal reservoirs to be taken into account in conservation issues.


Argentina Broussonetia papyrifera Celtis occidentalis Endophytes Ligustrum lucidum 



This study was financially supported by the Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad de Buenos Aires and Agencia Nacional de Promoción Científica y Tecnológica. We are grateful to Dr. Walter G., Friedrich-Schiller-Universitat, Germany, for assistance in the identification of Coprinus micaceus. PRHIDEB publication no. 177.


  1. Alves A, Crous PW, Correia A, Phillips AJL (2008) Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Divers 28:1–13Google Scholar
  2. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biological Reviews 21:51–56CrossRefGoogle Scholar
  3. Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Schnitzer S, Carson W (eds) Tropical forest community ecology. Blackwell Scientific, Inc, pp 254–271Google Scholar
  4. 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 95:388–398CrossRefGoogle Scholar
  5. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549CrossRefPubMedGoogle Scholar
  6. Arnold AE, Mejía L, Kyllo D, Rojas E, Maynard Z, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654CrossRefPubMedGoogle Scholar
  7. 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 99:185–206CrossRefPubMedGoogle Scholar
  8. Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:224–239CrossRefGoogle Scholar
  9. Bae H, Sicher RC, Kim MS, Kim S-H, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295CrossRefPubMedGoogle Scholar
  10. Barber PA, Burgess TI (2006) Three new Lasiodiplodia spp. from the tropics, recognized based on DNA sequence comparisons and morphology. Mycologia 98:423–435CrossRefPubMedGoogle Scholar
  11. Barklund P, Kowalski T (1996) Endophytic fungi in branches of Norway spruce with particular reference to Tryblidiopsis pinastri. Can J Bot 74:673–678CrossRefGoogle Scholar
  12. Boddy L, Rayner ADM (1983) Mycelial interactions, morphogenesis and ecology of Phlebia radiata and Phlebia rufa from oak. Tran Br Mycol Soc 80:437–448CrossRefGoogle Scholar
  13. Carmaran CC, Romero AI, Giussani LM (2006) An approach towards a new phylogenetic classification in Diatrypaceae. Fungal Divers 23:67–87Google Scholar
  14. Carroll GC, Wicklow DT (eds) (1992) The fungal community, its organization and role in the ecosystem, vol. 9. Dekker, New YorkGoogle Scholar
  15. Carroll GC, Müller E, Sutton BC (1977) Preliminary studies in the incidence of coniferous needle endophytes in the Pacific Northwest. Sydowia 29:87–103Google Scholar
  16. Chapela IH (1989) Fungi in healthy ítems and branches of American beech and aspen: a comparative study. New Phytol 113:65–75CrossRefGoogle Scholar
  17. Chapela IH, Boddy L (1988) Fungal colonization of attached beech branches. I. Early stages of development of fungal communities. New Phytol 110:39–45CrossRefGoogle Scholar
  18. Chudnoff M (1984) Tropical Timbers of the world. USDA Forest Service. Ag. Handbook Nº 607Google Scholar
  19. Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:1–16CrossRefGoogle Scholar
  20. Crous PW, Denman S, Taylor JE, Swart L, Palm ME (eds) (2004) Cultivation and diseases of proteaceae: Leucadendron, Leucospermum and Protea. CBS Biodiversity series 2, Utrech Netherlands. 126–132Google Scholar
  21. De Magistris AA (1996) Relevamiento florístico de Santa Catalina. Ed Fac de Cs Agrarias. UNLZGoogle Scholar
  22. Duong LM, Jeewon R, Lumyong SA, Hyde KD (2006) DGGE coupled with ribosomal DNA phylogenies reveal uncharacterized fungal phylotypos on living leaves of Magnolia lilifera. Fungal Divers 23:121–138Google Scholar
  23. Farr DF, Bills GF, Chamuris GP, Rosman AY (1989) Fungi on plants and plant products in the United States. APS, Minnesota, p 1325Google Scholar
  24. Fernandez Valiela MV (1978) Introducción a la fitopatología 3ra ed. Vol III: Hongos. INTA, Buenos Aires, p 330Google Scholar
  25. Fisher PJ, Petrini O, Petrini LE, Descals E (1992) A preliminary study of fungi inhabiting xylem and whole stems of Olea europaea. Sydowya 44:117–121Google Scholar
  26. Gams W, McGinnis MR (1983) Phialemonium, a new anamorph genus intermediate between Phialophora and Acremonium. Mycologia 75:977–987CrossRefGoogle Scholar
  27. 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 38:69–83Google Scholar
  28. Griffith GS, Boddy L (1990) Fungal decomposition of attached angiosperm twigs. Decay community development in ash, beach and oak. New Phytol 116:407–415CrossRefGoogle Scholar
  29. Hendry SJ, Boddy L, Lonsdale D (2002) Abiotic variables effect differential expression of latent infections in beech (Fagus sylvatica). New Phytol 155:449–460CrossRefGoogle Scholar
  30. Hoff JA, Klopfenstein NB, McDonald GI, Tonn JR, Kim M-S, Zambino PJ, Hessburg PF, Rogers JD, Peever TL, Carris LM (2004) Fungal endophytes in woody roots of Douglas-fir (Pseudotsuga menziesii) and ponderosa pine (Pinus ponderosa). For Pathol 34:255–271Google Scholar
  31. Huang WY, Cai YZ, Hyde KD, Corke H, Sun M (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61–75Google Scholar
  32. 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 36:69–88Google Scholar
  33. Hutchison LJ (1999) Wood-inhabiting microfungi isolated from Populus tremuloides from Alberta and northeastern British Columbia. Can J Bot 77:898–905CrossRefGoogle Scholar
  34. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  35. Iannone LJ, Cabral D (2006) Effects of the Neotyphodium endophyte status on plant performance of Bromus auleticus, a wild negative grass from South America. Symbiosis 41:61–69CrossRefGoogle Scholar
  36. IMBIAR (2006) Database on biological invasions in Argentina,
  37. Kowalski T, Kehr RD (1992) Endophytic fungal colonization of branch bases in several forest tree species. Sydowia 44:137–168Google Scholar
  38. Küffer N, Senn-Irlet B (2005) Influence of forest management on the species richness and composition of wood-inhabiting basidiomycetes in Swiss forests. Biodivers Conserv 14:2419–2435CrossRefGoogle Scholar
  39. Kumaresan V, Suryanarayanan TS (2002) Endophyte assemblages in young, mature and senescent leaves of Rhizophora apiculata: evidence for the role of endophytes in mangrove litter degradation. Fungal Divers 9:81–91Google Scholar
  40. Kvas M, Marasas WFO, Wingfield BD, Wingfield MJ, Steenkamp ET (2009) Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Divers 34:1–21Google Scholar
  41. 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
  42. Lazzizera C, Frisullo S, Alves A, Lopes J, Phillips AJL (2008) Phylogeny and morphology of Diplodia species on olives in southern Italy and description of Diplodia olivarum sp. nov. Fungal Divers 31:63–71Google Scholar
  43. Llic J, Boland D, McDonald M, Downes G, Blakemore P (2000) Wood density Phase 1. National carbon accounting system technical report Nº18. Australian Greenhouse Office, CanberraGoogle Scholar
  44. Mbogga MS (2001) Population dynamics and invasive potential of Broussonetia papyrifera (L.) Vert., in Budongo Forest Reserve, Uganda. Unpublished M.Sc. thesis, Makerere University, KampalaGoogle Scholar
  45. Miller DJ, Cherid H, Sumarah MW, Adams GW (2009) Horizontal transmission of the Picea glauca foliar endophyte Phialocephala scopiformis CBS 120377. Fungal Ecol 2:98–101CrossRefGoogle Scholar
  46. Nordén B, Ryberg M, Gotmark F, Olausson B (2004) Relative importance of coarse and fine woody debris for the diversity of wood-inhabitating fungi in temperate broadleaf forests. Biol Conserv 117:1–10CrossRefGoogle Scholar
  47. Novas MV, Carmarán CC (2008) Studies on diversity of foliar fungal endophytes of naturalised trees from Argentina, with a description of Haplotrichum minutissimum sp. nov. Flora 203:610–616Google Scholar
  48. Novas MV, Gentile A, Cabral D (2003) Comparative study of growth parameters between populations of Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30Google Scholar
  49. Novas MV, Cabral D, Godeas AM (2005) Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30Google Scholar
  50. Novas MV, Collantes M, Cabral D (2007) Environmental effects on grass–endophyte associations in the harsh conditions of south Patagonia. FEMS Microbiol Ecol 61:164–173CrossRefPubMedGoogle Scholar
  51. Oses R, Valenzuela S, Freer J, Baeza J, Rodriguez J (2006) Evaluation of fungal endophytes for lignocellulolytic enzyme production and wood biodegradation. Int Biodeterior Biodegradation 57:129–135CrossRefGoogle Scholar
  52. Oses R, Valenzuela S, Freer J, Sanfuentes E, Rodriguez J (2008) Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Divers 33:77–86Google Scholar
  53. Petrini O, Fisher PJ (1988) A comparative study of fungal endophytes in xylem and whole stem of Pinus sylvestris and Fagus sylvatica. Trans Br Mycol Soc 91:233–238CrossRefGoogle Scholar
  54. Phillips AJL, Crous PW, Alves A (2007) Diplodia seriata, the anamorph of “Botryosphaeria” obtusa. Fungal Divers 25:141–155Google Scholar
  55. Photita W, Lumyong S, Lumyong P, McKenzie EHC, Hyde KD (2004) Are some endophytes of Musa acuminata latent pathogens. Fungal Divers 16:131–140Google Scholar
  56. Photita W, Taylor PWJ, Ford R, Hyde KD, Lumyong S (2005) Morphological and molecular characterization of Colletotrichum species from herbaceous plants in Thailand. Fungal Divers 18:117–133Google Scholar
  57. Pitt JI (1997) Fungi and food spoilage, second edition. Blackie Academic & Professional, pp 108–147Google Scholar
  58. Ragazzi A, Moricca S, Capretti P, Dellavalle I, Turco E (2003) Differences in composition of endophytic mycobiota in twigs and leaves of healthy and declining Quercus species in Italy. For Pathol 33:31–38Google Scholar
  59. Raghukumar C (2008) Marine fungal biotechnology: an ecological perspective. Fungal Divers 31:19–35Google Scholar
  60. Rayner ADM (1986) Water and the origin of decay in trees. In: Ayres PG, Boddy L (eds) Water, fungi and plants. Cambridge University Press, Cambridge, pp 321–341Google Scholar
  61. Redhead SA, Vilgalys R, Moncalvo JM, Johnson J, Hopple JS Jr (2001) Coprinus Pers. and the disposition of Coprinus species sensu lato. Taxon 50:234Google Scholar
  62. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 22:1581CrossRefGoogle Scholar
  63. Renvall P (1995) Community structure and dynamics of wood-rotting basidiomycetes on decomposing conifer trunks in northern Finland. Karstenia 35:1–51Google Scholar
  64. Rifai MA (1969) A revision of the genus Trichoderma. Mycol pap 116:31–34Google Scholar
  65. Ribichich AL, Lopez SE (1996) Fungal decay in creosote-treated Eucalyptus power transmission poles. II Tolerance of soft rot fungi and related species from Argentina. Mat Org 30:63–72Google Scholar
  66. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330CrossRefPubMedGoogle Scholar
  67. Romero AI (1998) Clave de las especies de micromicetes xilófilos, registrados sobre Eucalyptus Viminalis Labill. en el NE de la provincia de Buenos Aires (Argentina). Bol Soc Micol de Madrid 23:47–89Google Scholar
  68. Romero AI, Minter D (1988) Fluorescence microscopy: an aid to the elucidation of Ascomycetes structure. Trans Br Mycol Soc 90:457–470CrossRefGoogle Scholar
  69. Romero AI, Carmaran CC, Lorenzo LE (1999) A new species of Coniochaeta with a key to the species known in Argentina. Mycol Res 103:689–695CrossRefGoogle Scholar
  70. Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones EBG (2008) Molecular characterization of Basidiomycetous endophytes isolated from leaves, rachis, petioles of the oil palm, Elaeis guineensis in Thailand. Fungal Divers 33:139–161Google Scholar
  71. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Ann Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  72. Samuels GJ, Dodd SL, Bing-Sheng Lu, Petrini O, Schroers H, Druzhinina IS (2006) The Trichoderma koningii aggregate species. Stud Mycol 56:67–133CrossRefPubMedGoogle Scholar
  73. Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87–100Google Scholar
  74. Santamaría O, Díez JJ (2005) Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain. For Pathol 35:95–104Google Scholar
  75. Schipper MAA (1984) A revision of the genus Rhizopus. Stud Mycol 25:20–28Google Scholar
  76. Schulz BJE, Boyle CJC, Sieber TN (eds) (2006) Microbial root endophytes. Soil Biology Vol. 9. Springer-Verlag Berlin Heidelberg, pp 119–121Google Scholar
  77. Schwarze FWMR, Engels J, Mattheck C (2000) Fungal strategies of wood decay in trees. Springer, BerlinGoogle Scholar
  78. Seena S, Wynberg N, Bärlocher F (2008) Fungal diversity during leaf decomposition in a stream assessed through clone libraries. Fungal Divers 30:1–14Google Scholar
  79. Sieber T, Hugentobler C (1987) Endophytische pilze in Blättern und Ästen gesunder und geschädigter Bunchen (Fagus sylvatica L.). Eur J Plant Pathol 17:411–425Google Scholar
  80. Slippers B, Wingfield MJ (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews 21:90–106CrossRefGoogle Scholar
  81. Slippers B, Fourie G, Crous PW, Coutinho TA, Wingfield BD, Wingfield MJ (2004) Multiple gene sequences delimit Botryosphaeria australis sp. nov. from B. lutea. Mycologia 96:1030–1041CrossRefGoogle Scholar
  82. Sutton BC (1980) The Coelomycetes, pp 221–222Google Scholar
  83. 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 33:101–122Google Scholar
  84. Tejesvi MV, Tamhankar SA, Kini KR, Rao VS, Prakash HS (2009) Phylogenetic analysis of endophytic Pestalotiopsis species from ethnopharmaceutically important medicinal trees. Fungal Divers 38:167–183Google Scholar
  85. Toti L, Viret O, Horat G, Petrini O (1993) Detection of the endophyte Discula umbrinella in buds and twigs of Fagus sylvatica. Eur J Plant Pathol 23:147–152Google Scholar
  86. Wagner BL, Lewis LC (2000) Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 66:3468–3473CrossRefPubMedGoogle Scholar
  87. Wang CJK, Zabel RA (eds) (1990) Identification manual for fungi from the utility poles in the eastern United States. Allen, MarylandGoogle Scholar
  88. Wilson D (1995) Endophyte—the evolution of a term, and clarification of its use and defifinition. Oikos 73:274–276CrossRefGoogle Scholar
  89. Wilson D (1996) Manipulation of infection levels of horizontally trasmitted fungal endophytes in the field. Mycol Res 100:827–830CrossRefGoogle Scholar
  90. Wright JE, Alberto E (2002) Hongos. Guía de la región pampeana. I. Hongos con laminillas. LOLA, Buenos Aires, p 168Google Scholar

Copyright information

© Kevin D Hyde 2010

Authors and Affiliations

  • A. de Errasti
    • 1
  • C. C. Carmarán
    • 1
  • M. Victoria Novas
    • 1
  1. 1.Lab. de Micología., Departamento de Biodiversidad y Biología Experimental (DBBE), Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations