Fungal Diversity

, Volume 60, Issue 1, pp 71–89 | Cite as

The endophytic mycobiota of Arabidopsis thaliana

  • Elena García
  • Ángela Alonso
  • Gonzalo Platas
  • Soledad Sacristán


Fungal endophytes are receiving increasing attention as resources to improve crop production and ecosystem management. However, the biology and ecological significance of these symbionts remains poorly understood, due to a lack of model systems for more efficient research. In this work, we have analyzed the culturable endophytic mycobiota associated, in the wild, with leaves and siliques of the model plant A. thaliana. We have studied the effect of biotic and abiotic factors in the frequency of fungal endophytes in plant specimens, and in the species composition of the endophytic community. Our results indicate that the frequency of Arabidopsis plants hosting endophytes depends on the time of the year and the phenological stage of the plant, and that the probability of endophyte colonization increases as the life cycle of the plant progresses. The diversity of the endophytic assemblages of natural A. thaliana populations was high, and precipitation and temperature were the two main factors determining the diversity and species composition of the communities. We propose A. thaliana and its endophytes as a model system for an integral approach to the principles governing the endophytic lifestyle, taking advantage of the molecular tools and the abundant knowledge accessible from the host plant.


Endophyte Mycobiota Arabidopsis Wild populations Ecology 



We thank Drs. Carlos Alonso-Blanco and Fernando García-Arenal for showing us the localization of the wild populations of A. thaliana. We also thank Drs. Fernando García-Arenal, and Mª Ángeles Ayllón, and an anonymous reviewer, for critical review and suggestions for improving the manuscript. Mª Ángeles Portal provided excellent technical assistance. Meteorological data have been gently provided by the Spanish Metereology Agency (AEMET). This work was funded by grants CAM CCG07-UPM/GEN-1899 of DGUI of Comunidad de Madrid and UPM and AGL2008-00818 of Ministerio de Educación y Ciencia of the Spanish Government to Soledad Sacristán.

Supplementary material

13225_2012_219_MOESM1_ESM.pdf (176 kb)
Online Resource 1 Bayesian consensus tree of the ITS1-5.8S rRNA-ITS2 sequence region of 120 fungal endophytic isolates of the different populations of A. thaliana. Only bootstrap values above 80 are shown. (PDF 175 kb)


  1. AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  2. Alcazar R, Parker J (2011) The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 16:666–675. doi: 10.1016/j.tplants.2011.09.001 PubMedCrossRefGoogle Scholar
  3. Aly A, Debbab A, Proksch P (2011a) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845. doi: 10.1007/s00253-011-3270-y PubMedCrossRefGoogle Scholar
  4. Aly A, Debbab A, Proksch P (2011b) Fifty years of drug discovery from fungi. Fungal Divers 50:3–19. doi: 10.1007/s13225-011-0116-y CrossRefGoogle Scholar
  5. Anderson JT, Mitchell-Olds T (2011) Ecological genetics and genomics of plant defences: evidence and approaches. Funct Ecol 25:312–324. doi: 10.1111/j.1365-2435.2010.01785.x PubMedCrossRefGoogle Scholar
  6. Arhipova N, Gaitnieks T, Donis J, Stenlid J, Vasaitis R (2011) Decay, yield loss and associate fungi in stands of grey alder (Alnus incana) in Latvia. Forestry 84:337–348CrossRefGoogle Scholar
  7. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. doi: 10.1016/j.fbr.2007.05.003 CrossRefGoogle Scholar
  8. Arnold A, Herre E (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398. doi: 10.2307/3761880 PubMedCrossRefGoogle Scholar
  9. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549. doi: 10.1890/05-1459 PubMedCrossRefGoogle Scholar
  10. Baynes M, Newcombe G, Dixon L, Castlebury L, O’Donnell K (2012) A novel plant fungal mutualism associated with fire. Fungal Biol 116:133–144PubMedCrossRefGoogle Scholar
  11. Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401PubMedCrossRefGoogle Scholar
  12. Bergelson J, Roux F (2010) Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat Rev Genet 11:867–879. doi: 10.1038/nrg2896 PubMedCrossRefGoogle Scholar
  13. Botella L, Diez J (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18. doi: 10.1007/s13225-010-0061-1 CrossRefGoogle Scholar
  14. Boyes D, Zayed A, Ascenzi R, McCaskill A, Hoffman N (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510. doi: 10.2307/3871382 PubMedGoogle Scholar
  15. Braun U, Crous PW, Dugan F, Groenewald JZ, De Hoog GS (2003) Phylogeny and taxonomy of Cladosporium-like hyphomycetes, including Davidiella gen. nov., the teleomorph of Cladosporium s. str. Mycol Prog 2:3–18CrossRefGoogle Scholar
  16. Bukovska P, Jelinkova M, Hrselova H, Sykorova Z, Gryndler M (2010) Terminal restriction fragment length measurement errors are affected mainly by fragment length, G+C nucleotide content and secondary structure melting point. J Microbiol Methods 82:223–228Google Scholar
  17. Bulgarelli D, Rott M, Schlaeppi K, Ahmadinejad N et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. doi: 10.1038/nature11336 PubMedCrossRefGoogle Scholar
  18. Caesar AJ, Lartey RT, Caesar-Ton-That T-C (2012) First report of a root and crown disease of the invasive weed Lepidium draba caused by Phoma macrostoma. Plant Dis 96:145CrossRefGoogle Scholar
  19. Cai L, Jeewon R, Hyde KD (2006) Phylogenetic investigations of Sordariaceae based on multiple gene sequences and morphology. Mycol Res 110:137–150PubMedCrossRefGoogle Scholar
  20. Cannon PF, Buddie AG, Bridge PD, de Neergaard E, Lubeck M, Askar MM (2012a) Lectera, a new genus of the Plectosphaerellaceae for the legume pathogen Volutella colletotrichoides. MycoKeys 3:23–36CrossRefGoogle Scholar
  21. Cannon PF, Damm U, Johnston PR, Weir BS (2012b) Colletotrichum – current status and future directions. Stud Mycol 73:181–213PubMedCrossRefGoogle Scholar
  22. Carroll G (1988) Fungal endophytes in stems and leaves - from latent pathogen to mutualistic symbiont. Ecology 69:2–9. doi: 10.2307/1943154 CrossRefGoogle Scholar
  23. Carroll G, Carroll F (1978) Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Can J Bot 56:3034–3043CrossRefGoogle Scholar
  24. Chaverri P, Castlebury LA, Samuels GJ, Geisera DM (2003) Multilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. Mol Phylogenet Evol 27:302–313PubMedCrossRefGoogle Scholar
  25. Colwell RK (2005) EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.0. Scholar
  26. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727CrossRefGoogle Scholar
  27. Compant S, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73:197–214. doi: 10.1111/j.1574-6941.2010.00900.x PubMedGoogle Scholar
  28. Cook D, Shi L, Gardner D, Pfister J, Grum D (2012) Influence of phenological stage on swainsonine and endophyte concentrations in Oxytropis sericea. J Chem Ecol 38:195–203. doi: 10.1007/s10886-012-0067-0 PubMedCrossRefGoogle Scholar
  29. Crous PW, Groenewald JZ (2011) Why everlastings don’t last. Persoonia 26:70–84PubMedCrossRefGoogle Scholar
  30. Crous PW, Summerell BA, Swart L, Denman S, Taylor JE, Bezuidenhout CM, Palm ME, Marincowitz S, Groenewald JZ (2011) Fungal pathogens of proteaceae. Persoonia 27:20–45PubMedCrossRefGoogle Scholar
  31. Cunnington (2004) Three Neofabraea species on pome fruit in Australia. Australas Plant Pathol 33:453–454CrossRefGoogle Scholar
  32. Damm U, Woudenberg JHC, Cannon PF, Crous PW (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Divers 39:45–87Google Scholar
  33. Davis EC, Shaw AJ (2008) Biogeographic and phylogenetic patterns in diversity of liverwort-associated endophytes. Am J Bot 95:914–924PubMedCrossRefGoogle Scholar
  34. Debbab A, Aly AH, Proksch P (2011) Bioactive secondary metabolites from endophytes and associated marine derived fungi. Fungal Divers 49:1–12. doi: 10.1007/s13225-011-0114-0 CrossRefGoogle Scholar
  35. Debbab A, Aly AH, Proksch P (2012) Endophytes and associated marine derived fungi—ecological and chemical perspectives. Fungal Divers 57:45–83. doi: 10.1007/s13225-012-0191-8 CrossRefGoogle Scholar
  36. Ehrhardt D, Frommer W (2012) New technologies for 21st century plant science. Plant Cell 24:374–394. doi: 10.1105/tpc.111.093302 PubMedCrossRefGoogle Scholar
  37. Escoufier Y, Roberts P (1979) Choosing variables and metrics by optimizing the RV coefficient. In: Rustagi JS (ed) Optimizing methods in statistics. Academic, New York, pp 205–219Google Scholar
  38. Farr DF, Aime MC, Rossman AY, Palm ME (2006) Species of Colletotrichum on agavaceae. Mycol Res 110:1395–1408PubMedCrossRefGoogle Scholar
  39. Feldman T, Morsy M, Roossinck M (2012) Are communities of microbial symbionts more diverse than communities of macrobial hosts? Fungal Biol 116:465–477. doi: 10.1016/j.funbio.2012.01.005 PubMedCrossRefGoogle Scholar
  40. Freeman S, Horowitz S, Sharon A (2001) Pathogenic and nonpathogenic lifestyles in Colletotrichum acutatum from strawberry and other plants. Phytopathology 91:986–992. doi: 10.1094/PHYTO.2001.91.10.986 PubMedCrossRefGoogle Scholar
  41. Fuhrman J (2009) Microbial community structure and its functional implications. Nature 459:193–199. doi: 10.1038/nature08058 PubMedCrossRefGoogle Scholar
  42. Gonzalez V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in Central Spain. Fungal Divers 47:29–42. doi: 10.1007/s13225-010-0073-x CrossRefGoogle Scholar
  43. Guo LD, Wang Y (2008) Seasonal and tissue age influences on endophytic fungi of Pinus tabulaeformis (Pinaceae) in the Dongling Mountains, Beijing. J Integr Plant Biol 50(8):997–1003PubMedCrossRefGoogle Scholar
  44. Hamilton C, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10. doi: 10.1007/s13225-012-0158-9 CrossRefGoogle Scholar
  45. Han G, Feng X, Tian X (2011) Isolation and evaluation of terrestrial fungi with algicidal ability from Zijin Mountain, Nanjing, China. J Microbiol 49:562–567PubMedCrossRefGoogle Scholar
  46. Hartmann M, Lee S, Hallam SJ, Mohn WW (2009) Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environ Microbiol 11:3045–3062PubMedCrossRefGoogle Scholar
  47. Herre E, Mejia L, Kyllo D, Rojas E, Maynard Z (2007) Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88:550–558. doi: 10.1890/05-1606 PubMedCrossRefGoogle Scholar
  48. Higgins KL, Arnold AE, Miadlikowska J, Sarvate S, Lutzoni F (2007) Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages. Mol Phylogenet Evol 42:543–555. doi: 10.1016/j.ympev.2006.07.012 PubMedCrossRefGoogle Scholar
  49. Hoffman M, Arnold AE (2008) Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees. Mycol Res 112:331–344. doi: 10.1016/j.mycres.2007.10.014 PubMedCrossRefGoogle Scholar
  50. Hoffmann M (2002) Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). J Biogeogr 29:125–134. doi: 10.1046/j.1365-2699.2002.00647.x CrossRefGoogle Scholar
  51. Hoyos-Carvajal L, Orduz S, Bissett J (2009) Genetic and metabolic biodiversity of Trichoderma from Colombia and adjacent neotropic regions. Fungal Genet Biol 46:615–631PubMedCrossRefGoogle Scholar
  52. Huelsenbeck JP, Joyce P, Lakner C, Ronquist F (2008) Bayesian analysis of amino acid substitution models. Philos Trans R Soc B-Biol Sci 363:3941–3953. doi: 10.1098/rstb.2008.0175 CrossRefGoogle Scholar
  53. Hyde K, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  54. Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW et al (2009) Colletotrichum – names in current use. Fungal Divers 39:147–182Google Scholar
  55. Jaschke D, Dugassa-Gobena D, Karlovsky P, Vidal S, Ludwig-Muller J (2010) Suppression of clubroot (Plasmodiophora brassicae) development in Arabidopsis thaliana by the endophytic fungus Acremonium alternatum. Plant Pathol 59:100–111CrossRefGoogle Scholar
  56. Johnston PR, Johansen RB, Williams AF, Paula Wikie J, Park D (2012) Patterns of fungal diversity in New Zealand Nothofagus forests. Fungal Biol 116:401–412PubMedCrossRefGoogle Scholar
  57. Junker C, Draeger S, Schulze B (2012) A fine line-endophytes or pathogens in Arabidopsis thaliana. Fungal Ecol 5:657–662. doi: 10.1016/j.funeco.2012.05.002 CrossRefGoogle Scholar
  58. Keurentjes JJB, Angenent G, Dicke M, Molenaar J (2011) Redefining plant systems biology: from cell to ecosystem. Trends Plant Sci 16:183–190. doi: 10.1016/j.tplants.2010.12.002 PubMedCrossRefGoogle Scholar
  59. Knief C, Ramette A, Frances L, Alonso Blanco C, Vorholt J (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J 4:719–728. doi: 10.1038/ismej.2010.9 PubMedCrossRefGoogle Scholar
  60. Kniskern J, Traw MB, Bergelson J (2007) Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana. Mol Plant-Microbe Interact 20:1512–1522. doi: 10.1094/MPMI-20-12-1512 PubMedCrossRefGoogle Scholar
  61. Ko Ko TW, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120. doi: 10.1007/s13225-011-0130-0 CrossRefGoogle Scholar
  62. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921. doi: 10.1111/j.1365-313X.2009.04086.x PubMedCrossRefGoogle Scholar
  63. Kuhnert R, Oberkofler I, Peintner U (2012) Fungal growth and biomass development is boosted by plants in snow-covered soil. Microb Ecol 64:79–90PubMedCrossRefGoogle Scholar
  64. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163. doi: 10.1093/bib/5.2.150 PubMedCrossRefGoogle Scholar
  65. Larkin BG, Hunt LS, Ramsey PW (2012) Foliar nutrients shape fungal endophyte communities in Western white pine (Pinus monticola) with implications for white-tailed deer herbivory. Fungal Ecol 5:252–260CrossRefGoogle Scholar
  66. Lawrence DP, Park MS, Pryor BM (2012) Nimbya and Embellisia revisited, with nov. comb for Alternaria celosiae and A. perpunctulata. Mycol Prog 11:799–815CrossRefGoogle Scholar
  67. Li H, Wei D, Shen M, Zhou Z (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18. doi: 10.1007/s13225-012-0165-x CrossRefGoogle Scholar
  68. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620PubMedCrossRefGoogle Scholar
  69. Lindner DL, Vasaitis R, Kubartova A, Allmer J, Johannesson H, Banik MT, Stenlid J (2011) Initial fungal colonizer affects mass loss and fungal community development in Picea abies logs 6 yr after inoculation. Fungal Ecol 4:449–460CrossRefGoogle Scholar
  70. Lorch JM, Lindner DL, Gargas A, Muller LK, Minnis AM, Blehert DS (2012) Mycologia 12–207Google Scholar
  71. Lu G, Cannon P, Reid A, Simmons C (2004) Diversity and molecular relationships of endophytic Colletotrichum isolates from the Iwokrama Forest Reserve, Gruyana. Mycol Res 108:53–63. doi: 10.1017/S0953756203008906 PubMedCrossRefGoogle Scholar
  72. Lundberg D, Lebeis S, Paredes S, Yourstone S, Gehring J et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86. doi: 10.1038/nature11237 PubMedCrossRefGoogle Scholar
  73. Macia-Vicente JG, Ferraro V, Burruano S, Lopez-Llorca LV (2012) Fungal assemblages associated with roots of halophytic and non-halophytic plant species vary differentially along a salinity gradient. Microb Ecol 64:668–679PubMedCrossRefGoogle Scholar
  74. Magurran AE (2004) Measuring biological diversity. Blackwell Publishing, OxfordGoogle Scholar
  75. Mehta YR, Mehta A, Rosato YB (2002) ERIC and REP-PCR banding patterns and sequence analysis of the Internal Transcribed Spacer of rDNA of Stemphylium solani isolates from cotton. Curr Microbiol 44:323–328PubMedCrossRefGoogle Scholar
  76. Micallef S, Shiaris M, Colon Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742. doi: 10.1093/jxb/erp053 PubMedCrossRefGoogle Scholar
  77. Mirabolfathy M, Groenewald JZ, Crous PW (2011) The occurrence of charcoal disease caused by Biscogniauxia mediterranea on chestnut-leaved oak (Quercus castaneifolia) in the Golestan Forests of Iran. Plant Dis 95:876CrossRefGoogle Scholar
  78. Mishra A, Gond S, Kumar A, Sharma V, Verma S (2012) Season and tissue type affect fungal endophyte communities of the Indian medicinal plant Tinospora cordifolia more strongly than geographic location. Microb Ecol 64:388–398. doi: 10.1007/s00248-012-0029-7 PubMedCrossRefGoogle Scholar
  79. Morales VM, Pelcher LE, Taylor JL (1993) Comparison of the 5.8 s rDNA and internal transcribed spacer sequences of isolates of Leptosphaeria maculans from different pathogenicity groups. Curr Genet 23:490–495PubMedCrossRefGoogle Scholar
  80. Muller LK, Lorch JM, Lindner DL, O’Connor M, Gargas A, Blehert DS (2012) Bat white-nose syndrome: a real-time TaqMan polymerase chain reaction test targeting the intergenic spacer region of Geomyces destructans. Mycologia In pressGoogle Scholar
  81. Neubert K, Mendgen K, Brinkmann H, Wirsel S (2006) Only a few fungal species dominate highly diverse mycofloras associated with the common reed. Appl Environ Microbiol 72:1118–1128. doi: 10.1128/AEM.72.2.1118-1128.2006 PubMedCrossRefGoogle Scholar
  82. Nirenberg HI, Feiler U, Hagedorn G (2002) Description of Colletotrichum lupini comb. nov. in modern terms. Mycologia 94:307–320PubMedCrossRefGoogle Scholar
  83. Nishimura M, Dangl J (2010) Arabidopsis and the plant immune system. Plant J 61:1053–1066. doi: 10.1111/j.1365-313X.2010.04131.x PubMedCrossRefGoogle Scholar
  84. O’Connell R, Herbert C, Sreenivasaprasad S, Khatib M, Esquerré-Tugayé M-T, Dumas M (2004) A novel arabidopsiscolletotrichum pathosystem for the molecular dissection of plant–fungal interactions. MPMI 17:272–282PubMedCrossRefGoogle Scholar
  85. O’Connell R, Thon M, Hacquard S, Amyotte S, Kleemann J et al (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44:1060. doi: 10.1038/ng.2372 PubMedCrossRefGoogle Scholar
  86. O’Donnell K, Gray LE (1995) Phylogenetic relationships of the soybean sudden death syndrome pathogen Fusarium solani f. sp. phaseoli inferred from rDNA sequence data and PCR primers for its identification. Mol Plant Microbe Interact 8:709–716PubMedCrossRefGoogle Scholar
  87. Osono T (2008) Endophytic and epiphytic phyllosphere fungi of Camellia japonica: seasonal and leaf age-dependent variations. Mycologia 100:387–391PubMedCrossRefGoogle Scholar
  88. Pagan I, Fraile A, Fernandez-Fueyo E, Montes N, Alonso-Blanco C, Garcia-Arenal F (2010) Arabidopsis thaliana as a model for the study of plant-virus co-evolution. Phil Trans R Soc B Biol Sci 365:1983–1995CrossRefGoogle Scholar
  89. Partfitt D, Hunt J, Dockrell D, Rogers HJ, Boddy L (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 3:338–346CrossRefGoogle Scholar
  90. Peskan Berghofer T, Shahollari B, Giong P, Hehl S, Markert C et al (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plantarum 122:465–477. doi: 10.1111/j.1399-3054.2004.00424.x CrossRefGoogle Scholar
  91. Pico FX, Mendez Vigo B, Martinez Zapater J, Alonso Blanco C (2008) Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian Peninsula. Genetics 180:1009–1021. doi: 10.1534/genetics.108.089581 PubMedCrossRefGoogle Scholar
  92. Porras Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315PubMedCrossRefGoogle Scholar
  93. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi: 10.1080/10635150490522304 PubMedCrossRefGoogle Scholar
  94. Purahong W, Hyde KD (2011) Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7. doi: 10.1007/s13225-010-0083-8 CrossRefGoogle Scholar
  95. Qi FH, Jing TZ, Wang ZX, Zhan YG (2009) Fungal endophytes from Acer ginnala Maxim: isolation, identification and their yield of gallic acid. Lett Appl Microbiol 49:98–104PubMedCrossRefGoogle Scholar
  96. Rakotoniriana EF, Munaut F, Decock C, Randriamampionona D, Andriambololoniaina M (2008) Endophytic fungi from leaves of Centella asiatica: occurrence and potential interactions within leaves. Antonie Van Leeuwenhoek 93:27–36. doi: 10.1007/s10482-007-9176-0 PubMedCrossRefGoogle Scholar
  97. Ramos B, González-Melendi P, Sánchez-Vallet A, Sánchez-Rodríguez C, López G, Molina A (2013) Functional genomics tools to decipher the pathogenicity mechanisms of the necrotrophic fungus Plectosphaerella cucumerina in Arabidopsis thaliana. Mol Plant Pathol 14:44–57. doi: 10.1111/j.1364-3703.2012.00826.x PubMedCrossRefGoogle Scholar
  98. Redman R, Dunigan D, Rodriguez R (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716. doi: 10.1046/j.0028-646x.2001.00210.x CrossRefGoogle Scholar
  99. Redondo C, Cubero J, Melgarejo P (2009) Characterization of Penicillium species by ribosomal DNA sequencing and BOX, ERIC and REP-PCR analysis. Mycopathologia 168:11–22PubMedCrossRefGoogle Scholar
  100. Rivera-Orduna FN, Suarez-Sanchez RA, Flores-Bustamante ZR, Gracida-Rodriguez JN, Flores-Cotera LB (2011) Diversity of endophytic fungi of Taxus globosa (Mexican yew). Fungal Divers 47:65–74. doi: 10.1007/s13225-010-0045-1 CrossRefGoogle Scholar
  101. Rodrigues A, Mueller UG, Ishak HD, Bacci M Jr, Pagnocca FC (2011) Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species of attine ants in Central Texas. FEMS Microbiol Ecol 78:244–255PubMedCrossRefGoogle Scholar
  102. Rodriguez R, White J, Arnold A, Redman R (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedCrossRefGoogle Scholar
  103. Rojas E, Rehner S, Samuels G, Van Bael S, Herre E (2010) Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102:1318–1338. doi: 10.3852/09-244 PubMedCrossRefGoogle Scholar
  104. Ronquist F, Huelsenbeck J (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi: 10.1093/bioinformatics/btg180 PubMedCrossRefGoogle Scholar
  105. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74. doi: 10.1016/j.fbr.2007.05.001 CrossRefGoogle Scholar
  106. Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113. doi: 10.1007/s13225-010-0023-7 CrossRefGoogle Scholar
  107. Salvaudon L, Giraud T, Shykoff J (2008) Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Curr Opin Plant Biol 11:135–143PubMedCrossRefGoogle Scholar
  108. Sanchez Marquez S, Bills G, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195Google Scholar
  109. Sanchez Marquez S, Bills GF, Dominguez Acuna L, Zabalgogeazcoa I (2010) Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fungal Divers 41:115–123. doi: 10.1007/s13225-009-0015-7 CrossRefGoogle Scholar
  110. Sanchez Marquez S, Bills G, Herrero N, Zabalgogeazcoa I (2012) Non-systemic fungal endophytes of grasses. Fungal Ecol 5:289–297. doi: 10.1016/j.funeco.2010.12.001 CrossRefGoogle Scholar
  111. Saunders M, Glenn A, Kohn L (2010) Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3:525–537. doi: 10.1111/j.1752-4571.2010.00141.x CrossRefGoogle Scholar
  112. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686. doi: 10.1017/S095375620500273X PubMedCrossRefGoogle Scholar
  113. Schulz B, Wanke U, Draeger S, Aust H (1993) Endophytes from herbaceous plants and shrubs - effectiveness of surface sterilization methods. Mycol Res 97:1447–1450CrossRefGoogle Scholar
  114. Sen R, Ishak HD, Estrada D, Dowd SE, Hong E, Mueller UG (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci USA 106:17805–17810PubMedCrossRefGoogle Scholar
  115. Shanmugam V, Dhyani D, Ananthapadmanaban D (2011) First report of Alternaria sp. causing blight on Incarvillea emodi. Australas Plant Dis Notes 6:33–35CrossRefGoogle Scholar
  116. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  117. Shrestha P, Szaro TM, Bruns TD, Taylor JW (2011) Systematic search for cultivatable fungi that best deconstruct cell walls of Miscanthus and sugarcane in the field. Appl Environ Microbiol 77:5490–5504PubMedCrossRefGoogle Scholar
  118. Sieber T (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75. doi: 10.1016/j.fbr.2007.05.004 CrossRefGoogle Scholar
  119. Simon UK, Weiss M (2008) Intragenomic variation of fungal ribosomal genes is higher than previously thought. Mol Biol Evol 25:2251–2254PubMedCrossRefGoogle Scholar
  120. Simon UK, Groenewald JZ, Crous PW (2009) Cymadothea trifolii, an obligate biotrophic leaf parasite of Trifolium, belongs to Mycosphaerellaceae as shown by nuclear ribosomal DNA analyses. Persoonia 22:49–55PubMedCrossRefGoogle Scholar
  121. Slemmons C, Johnson G, Connell LB (2012) Application of an automated ribosomal intergenic spacer analysis data base for identification of cultured Antarctic fungi. Antarct Sci In pressGoogle Scholar
  122. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Co, New YorkGoogle Scholar
  123. Stone JK (2006) Ecological roles of endophytes in forest ecosystems. Phytopathology 96:S136Google Scholar
  124. Sun X, Guo L-D (2008) Apsensculmus, a new genus and its phylogenetic placement based on molecular analysisGoogle Scholar
  125. Sun H, Zhang JZ (2009) Colletotrichum destructivum from cowpea infecting Arabidopsis thaliana and its identity to C. higginsianum. Eur J Plant Pathol 125:459–469CrossRefGoogle Scholar
  126. Suryanarayanan T, Murali T, Venkatesan G (2002) Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Can J Bot 80:818–826. doi: 10.1139/B02-069 CrossRefGoogle Scholar
  127. Suryanarayanan T, Venkatesan G, Murali T (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci 85:489–493Google Scholar
  128. Suryanarayanan T, Thirunavukkarasu N, Govindarajulu M, Gopalan V (2012) Fungal endophytes: an untapped source of biocatalysts. Fungal Divers 54:19–30. doi: 10.1007/s13225-012-0168-7 CrossRefGoogle Scholar
  129. Tadych M, Bergen M, Johnson Cicalese J, Polashock J, Vorsa N (2012) Endophytic and pathogenic fungi of developing cranberry ovaries from flower to mature fruit: diversity and succession. Fungal Divers 54:101–116. doi: 10.1007/s13225-012-0160-2 CrossRefGoogle Scholar
  130. Taylor J, Jacobson D, Kroken S, Kasuga T, Geiser D (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32. doi: 10.1006/fgbi.2000.1228 PubMedCrossRefGoogle Scholar
  131. Tejesvi M, Mahesh B, Nalini M, Prakash H, Kini K (2005) Endophytic fungal assemblages from inner bark and twig of Terminalia arjuna W. A. (Combretaceae). World J Microbiol Biotechnol 21:1535–1540. doi: 10.1007/s11274-005-7579-5 CrossRefGoogle Scholar
  132. Ter Braak CJF (1992) Permutation versus bootstrap significance tests in multiple regression and ANOVA. In: Jöckel KH, Rothe G, Sendler (eds) Bootstrapping and related techniques. Springer Verlag, Berlin, pp 79–85CrossRefGoogle Scholar
  133. Ter Braak CJF, Smilauer P (2002) CANOCO Reference Manual and CANODRAW for User’s Guide version 4.5., Ithaca, NYGoogle Scholar
  134. Ter Braak CJF, Verdonschot PFM (1995) Canoncal correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57:255–289CrossRefGoogle Scholar
  135. Terhonen E, Marco T, Sun H, Jalkanen R, Kasanen R (2011) The effect of latitude, season and needle-age on the mycota of Scots Pine (Pinus sylvestris) in Finland. Silva Fenn 45:301–317Google Scholar
  136. Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi: 10.1093/nar/25.24.4876 PubMedCrossRefGoogle Scholar
  137. Thongsandee W, Matsuda Y, Ito S (2012) Temporal variations in endophytic fungal assemblages of Ginkgo biloba L. J For Res 17:213–218. doi: 10.1007/s10310-011-0292-3 CrossRefGoogle Scholar
  138. Traw MB, Bergelson J (2010) Plant immune system incompatibility and the distribution of enemies in natural hybrid zones. Curr Opin Plant Biol 13:466–471. doi: 10.1016/j.pbi.2010.04.009 PubMedCrossRefGoogle Scholar
  139. 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 3:366–378CrossRefGoogle Scholar
  140. Wearn J, Sutton B, Morley N, Gange A (2012) Species and organ specificity of fungal endophytes in herbaceous grassland plants. J Ecol 100:1085–1092. doi: 10.1111/j.1365-2745.2012.01997.x CrossRefGoogle Scholar
  141. Weiss M, Sykorova Z, Garnica S, Riess K, Martos F (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS One 6. doi: 10.1371/journal.pone.0016793
  142. White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal genes for phylogenetics. PCR protocols: a guide of methods and applications 315–322Google Scholar
  143. Wilson D (1995) Endophyte - the evolution of a term, and clarification of its use and definition. Oikos 73:274–276. doi: 10.2307/3545919 CrossRefGoogle Scholar
  144. Wilson D (2000) Ecology of woody plant endophytes. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Marcel Dekker, New YorkGoogle Scholar
  145. Yuan ZL, Zhang CL, Lin FC, Kubicek CP (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 Microbiol 76:1642–1652PubMedCrossRefGoogle Scholar
  146. Yurkov AM, Schafer AM, Begerow D (2012) Leucosporidium drummii sp. nov., a member of the Microbotryomycetes isolated from soil. Int J Syst Evol Microbiol 62:728–734PubMedCrossRefGoogle Scholar
  147. Zak JC, Willig MR (2004) Fungal biodiversity patterns. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi. Inventory and monitoring methods. Elsevier Academic Press, USA, pp 59–75CrossRefGoogle Scholar
  148. Zak D, Pregitzer K, Burton A, Edwards I, Kellner H (2011) Microbial responses to a changing environment: implications for the future functioning of terrestrial ecosystems. Fungal Ecol 4:386–395. doi: 10.1016/j.funeco.2011.04.001 CrossRefGoogle Scholar
  149. Zimmerman N, Vitousek P (2012) Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci U S A 109:13022–13027. doi: 10.1073/pnas.1209872109 PubMedCrossRefGoogle Scholar

Copyright information

© Mushroom Research Foundation 2012

Authors and Affiliations

  • Elena García
    • 1
  • Ángela Alonso
    • 2
  • Gonzalo Platas
    • 3
  • Soledad Sacristán
    • 1
  1. 1.Centro de Biotecnología y Genómica de Plantas (UPM-INIA) and E.T.S.I. AgrónomosUniversidad Politécnica de Madrid, Campus de MontegancedoMadridSpain
  2. 2.Departamento de Biotecnología, E.T.S.I. AgrónomosUniversidad Politécnica de MadridMadridSpain
  3. 3.Fundación Centro de Excelencia en Investigación de Medicamentos Innovadores en Andalucía MEDINAParque Tecnológico de las Ciencias de la Salud de GranadaArmillaSpain

Personalised recommendations