Advertisement

Microbial Ecology

, Volume 75, Issue 1, pp 74–87 | Cite as

Host Specificity of Endophytic Mycobiota of Wild Nicotiana Plants from Arid Regions of Northern Australia

  • Khondoker M. G. Dastogeer
  • Hua Li
  • Krishnapillai Sivasithamparam
  • Michael G. K. Jones
  • Stephen J. Wylie
Fungal Microbiology

Abstract

In arid regions of northern Australia, plants survive under water deficit, high temperatures, intense solar radiation and nutrient-impoverished soils. They employ various morpho-physiological and biochemical adaptations including interaction with microbial symbionts. We evaluated identity, host and tissue association with geographical distribution of fungal endophytes isolated from above- and below-ground tissues of plants of three indigenous Australian Nicotiana species. Isolation frequency and α-diversity were significantly higher for root endophyte assemblages than those of stem and leaf tissues. We recorded no differences in endophyte species richness or diversity as a function of sampling location, but did detect differences among different host genotypes and plant tissues. There was a significant pattern of community similarity associated with host genotypes but no consistent pattern of fungal community structuring associated with sampling location and tissue type, regardless of the community similarity measurements used.

Keywords

Arid land Community structure Endophyte diversity Fungi 

Notes

Acknowledgements

The first author was supported through the Research Training Program (RTP) scheme (formerly known as the International Postgraduate Research Scholarship, IPRS) by Murdoch University, Australia.

Supplementary material

248_2017_1020_MOESM1_ESM.xlsx (37 kb)
Table S1 (XLSX 36 kb).
248_2017_1020_MOESM2_ESM.docx (164 kb)
Figure S1 (DOCX 163 kb).
248_2017_1020_MOESM3_ESM.docx (152 kb)
Figure S2 (DOCX 151 kb).
248_2017_1020_MOESM4_ESM.docx (114 kb)
Figure S3 (DOCX 113 kb).
248_2017_1020_MOESM5_ESM.txt (134 kb)
ESM 1 (TXT 133 kb).
248_2017_1020_MOESM6_ESM.txt (76 kb)
ESM 2 (TXT 75 kb).

References

  1. 1.
    Hopper SD, Brown AP, Marchant NG (1997) Plants of Western Australian granite outcrops. J. R. Soc. West. Aust. 80:141–158Google Scholar
  2. 2.
    Pepper M, Keogh JS (2014) Biogeography of the Kimberley Western Australia: a review of landscape evolution and biotic responses in an ancient refugium. J. Biogeogr. 41:1443–1445CrossRefGoogle Scholar
  3. 3.
    Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7:e48479CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14:1–4. doi: 10.1016/j.tplants.2008.10.004 CrossRefPubMedGoogle Scholar
  5. 5.
    Khidir HK, Eudy DM, Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2010) A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J. Arid Environ. 74:35–42. doi: 10.1016/j.jaridenv.2009.07.014 CrossRefGoogle Scholar
  6. 6.
    Lucero ME, Barrow JR, Osuna P, Reyes I (2006) Plant-fungal interactions in arid and semi-arid ecosystems: large-scale impacts from microscale processes. J. Arid Environ. 65:276–284CrossRefGoogle Scholar
  7. 7.
    Lugo MA, Reinhart KO, Menoyo E, Crespo EM, Urcelay C (2015) Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment. Mycorrhiza 25:85–95CrossRefPubMedGoogle Scholar
  8. 8.
    Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach K, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Appl. Environ. Microbiol. 74:2805–2813CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Herrera J, Khidir HH, Eudy DM, Porras-Alfaro A, Natvig DO, Sinsabaugh RL (2010) Shifting fungal endophyte communities colonize Bouteloua gracilis: effect of host tissue and geographical distribution. Mycologia 102:1012–1026CrossRefPubMedGoogle Scholar
  10. 10.
    Porras-Alfaro A, Raghavan S, Garcia M, Sinsabaugh RL, Natvig DO, Lowrey TK (2014) Endophytic fungal symbionts associated with gypsophilous plants. Bot 92:295–301CrossRefGoogle Scholar
  11. 11.
    Lucero ME, Unc A, Cooke P, Dowd S, Sun S (2011) Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. PLoS One 6:e17693CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol. Res. 109:635–639CrossRefPubMedGoogle Scholar
  13. 13.
    Bacon CW, White JF (2000) Microbial endophytes. CRC Press. Marcel Dekker Inc., New YorkGoogle Scholar
  14. 14.
    U'Ren JM, Dalling JW, Gallery RE, Maddison DR, Davis EC, Gibson CM, Arnold AE (2009) Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analyzing fungal environmental samples. Mycol. Res. 113:432–449CrossRefPubMedGoogle Scholar
  15. 15.
    Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biology Reviews 21:67–74CrossRefGoogle Scholar
  16. 16.
    Collado J, Platas G, González I, Peláez F (1999) Geographical and seasonal influences on the distribution of fungal endophytes in Quercus ilex. New Phytol. 144:525–532CrossRefGoogle Scholar
  17. 17.
    Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Divers. 17:69–90Google Scholar
  18. 18.
    Malinowski DP, Belesky DP (2000) Adaptations of endophtye-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci. 40:923–940CrossRefGoogle Scholar
  19. 19.
    Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl. Sci. 52:23–28CrossRefGoogle Scholar
  20. 20.
    Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig. Adapt. Strateg. Glob. Chang. 9:261–272CrossRefGoogle Scholar
  21. 21.
    Zabalgogeazcoa I (2008) Fungal endophytes and their interactions with plant pathogens. Span. J. Agric. Res. 6:138–146CrossRefGoogle Scholar
  22. 22.
    Lewis GC, Clement RO (1986) A survey of ryegrass endophyte in the U.K. and its apparent ineffectuality on a seedling pest. J. Agric. Sci. 107:633–638CrossRefGoogle Scholar
  23. 23.
    Rodriguez EAE, Jonkers W, Kistler HC, May G (2012) Interactions between Fusarium verticillioides, Ustilago maydis, and Zea mays: an endophyte, a pathogen, and their shared plant host. Fungal Genet. Biol. 49:578–587CrossRefGoogle Scholar
  24. 24.
    Higginbotham SJ, Arnold AE, Ibañez A, Spadafora C, Coley PD, Kursar TA (2013) Bioactivity of fungal endophytes as a function of endophyte taxonomy and the taxonomy and distribution of their host plants. PLoS One 8:e73192CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Rodriguez RJ, White J, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and ecological roles. New Phytol. 182:314–330CrossRefPubMedGoogle Scholar
  26. 26.
    Barrow JR, Osuna P (2002) Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. J. Arid Environ. 51:449–459CrossRefGoogle Scholar
  27. 27.
    Bezerra JDP, Santos MGS, Svedese VM, Lima DMM, Fernandes MJS, Paiva LM, Souza-Motta CM (2012) Richness of endophytic fungi isolated from Opuntia ficus-indica Mill. (Cactaceae) and preliminary screening for enzyme production. World J. Microbiol. Biotechnol. 28: 1989–1995.Google Scholar
  28. 28.
    Lopez BR, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the southern Sonoran Desert. Arch. Microbiol. 193:527–541CrossRefPubMedGoogle Scholar
  29. 29.
    Massimo NC, Nandi Devan MM, Arendt KR, Wilch MH, Riddle JM, Furr SH, Steen C, U'Ren JM, Sandberg DC, Arnold AE (2015) Fungal endophytes in aboveground tissues of desert plants: infrequent in culture, but highly diverse and distinctive symbionts. Microb. Ecol. 70:61–76. doi: 10.1007/s00248-014-0563-6 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol. 140:295–310. doi: 10.1046/j.1469-8137.1998.00265.x CrossRefGoogle Scholar
  31. 31.
    Porras-Alfaro A, Herrera J, Natvig DO, Lipinski K, Sinsabaugh RL (2011) Diversity and distribution of soil fungal communities in a semiarid grassland. Mycologia 103:10–21CrossRefPubMedGoogle Scholar
  32. 32.
    Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2007) Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant Soil 296:65–75. doi: 10.1007/ s11104-007-9290-9 CrossRefGoogle Scholar
  33. 33.
    Sun Y, Wang Q, Lu X, Okane I, Kakishima M (2012) Endophytic fungal community in stems and leaves of plants from desert areas in China. Mycol. Prog. 11:781–790CrossRefGoogle Scholar
  34. 34.
    Marks CE, Newbigin E, Ladiges PY (2011) Comparative morphology and phylogeny of Nicotiana section Suaveolentes (Solanaceae) in Australia and the South Pacific. Aust. Syst. Bot. 24:61–86CrossRefGoogle Scholar
  35. 35.
    Schulz B, Wanke U, Draeger S, Aust HJ (1993) Endophytes from herbaceous plants and shrubs: effectiveness of surfuse sterilization methods. Mycol. Res. 97:1447–1450CrossRefGoogle Scholar
  36. 36.
    Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect. 5:535–544CrossRefPubMedGoogle Scholar
  37. 37.
    Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol. Lett. 3:267–274CrossRefGoogle Scholar
  38. 38.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113–118CrossRefPubMedGoogle Scholar
  39. 39.
    White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Academic Press, New YorkGoogle Scholar
  40. 40.
    Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U (2010) The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytol. 186:281–285CrossRefPubMedGoogle Scholar
  41. 41.
    Rosa LH, Almeida Vieira Mde L, Santiago IF, Rosa CA (2010) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol. Ecol. 73:178–189PubMedGoogle Scholar
  42. 42.
    Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Humana Press, New JerseyCrossRefGoogle Scholar
  43. 43.
    Katoh K, Standley DM (2014) MAFFT: iterative refinement and additional methods. Methods Mol. Biol. 1079:131–146CrossRefPubMedGoogle Scholar
  44. 44.
    Kia SH, Glynou K, Nau T, Thines M, Piepenbring M, Maciá-Vicente JG (2017) Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants. The ISME journal 11:777–790. doi: 10.1038/ismej.2016.140 CrossRefPubMedGoogle Scholar
  45. 45.
    Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  46. 46.
    Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Wylie SJ, Zhang C, Long V, Roossinck MJ, Koh SH, Jones MGK, Iqbal S, Li H (2015) Differential responses to virus challenge of laboratory and wild accessions of Australian species of Nicotiana, and comparative analysis of RDR1 gene sequences. PLoS One 10:e0121787. doi: 10.1371/journal.pone.0121787 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Chung CL, Longfellow JM, Walsh EK, Kerdieh Z, Van Esbroeck G (2010) Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize–Setosphaeria turcica pathosystem. BMC Plant Biol. 10:103CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Colwell RK, Chao A, Gotelli NJ, Lin S-L, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 5:3–21CrossRefGoogle Scholar
  50. 50.
    Krebs CJ (1989) Ecological methodology. Harper & Row, New YorkGoogle Scholar
  51. 51.
    Quinn GP, Keough MJ (2002) Multidimensional scaling and cluster analysis. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  52. 52.
    Wolda H (1981) Similarity indices, sample size and diversity. Oecologia 50:296–302CrossRefPubMedGoogle Scholar
  53. 53.
    Fisher PJ, Petrini O, Petrini LE, Sutton BC (1994) Fungal endophytes from the leaves and twigs of Quercus ilex L. from England, Majorca and Switzerland. The New phytologist 127:133–147CrossRefGoogle Scholar
  54. 54.
    Gauch HG (1982) Multivariate analysis in community ecology. Cambridge University Press, CambridgeGoogle Scholar
  55. 55.
    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4:9Google Scholar
  56. 56.
    Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Melnick RL, Bailey BA (2011) Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Molecular plant-microbe interactions : MPMI 24:336–351CrossRefPubMedGoogle Scholar
  57. 57.
    Andrew DR, Fitak RR, Munguia-Vega A, Racolta A, Martinson VG, Dontsova K (2012) Abiotic factors shape microbial diversity in Sonoran Desert soils. Appl. Environ. Microbiol. 78:7527–7537CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers. 33:163–173Google Scholar
  59. 59.
    Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical trees biodiversity hot spots? Ecology 88:541–549CrossRefPubMedGoogle Scholar
  60. 60.
    Pinruan U, Rungjindamai N, Choeyklin R, Lumyong S, Hyde K, Jones E (2010) Occurrence and diversity of basidiomycetous endophytes from the oil palm, Elaeis guineensis in Thailand. Fungal Divers. 41:71–88CrossRefGoogle Scholar
  61. 61.
    Cai L, Hyde KD, Taylor PWJ, Weir BS, Waller J, Abang MM, Zhang JZ, Yang YL, Phoulivong S, Liu ZY, Prihastuti H, Shivas RG, McKenzie EHC, Johnston PR (2009) A polyphasic approach for studying Colletotrichum. Fungal Divers. 39:183–204Google Scholar
  62. 62.
    Blaalid R, Kumar S, Nilsson RH, Abarenkov K, Kirk PM (2013) ITS1 versus ITS2 as DNA metabarcodes for fungi. Mol. Ecol. Resour. 13:218–224CrossRefPubMedGoogle Scholar
  63. 63.
    Op De Beeck M, Lievens B, Busschaert P, Declerck S, Vangronsveld J, Colpaert JV (2014) Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS One 9:e97629CrossRefGoogle Scholar
  64. 64.
    U'Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host- and geographic structure of endophytic and endolichenic fungi at a continental scale. Am. J. Bot. 99:898–9143CrossRefPubMedGoogle Scholar
  65. 65.
    Sakayaroj J, Preedanon S, Supaphon O, Jones EBG, Phongpaichit S (2010) Phylogenetic diversity of endophyte assemblages associated with the tropical seagrass Enhalus acoroides in Thailand. Fungal Divers. 42:27–45CrossRefGoogle Scholar
  66. 66.
    Stone JK, Polishook JD, White JRJ (2004) Endophytic fungi. Elsevier, BurlingtonCrossRefGoogle Scholar
  67. 67.
    Thomas SE, Crozier J, Aime MC, Evans HC, Holmes KA (2008) Molecular characterization of fungal endophytic morphospecies associated with the indigenous forest tree, Theobroma gileri, in Ecuador. Mycol. Res. 112:852–860CrossRefPubMedGoogle Scholar
  68. 68.
    Albrectsen BR, Björkén L, Varad A, Hagner A, Wedin M, Karlsson J, Jansso S (2010) Endophytic fungi in European aspen (Populus tremula) leaves-diversity, detection, and a suggested correlation with herbivory resistance. Fungal Divers. 41. doi: 10.1007/s13225-009-0011-y
  69. 69.
    Zhang ZB, Zeng QG, Yan RM, Wang Y, Zou ZR, Zhu D (2011) Endophytic fungus Cladosporium cladosporioides LF70 from Huperzia serrata produces Huperzine A. World J. Microbiol. Biotechnol. 27:479–486CrossRefGoogle Scholar
  70. 70.
    Botella L, Diez JJ (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
  71. 71.
    Cannon CD, Simmons CM (2002) Diversity and host preference of leaf endophytic fungi in the Iwokrama forest reserve, Guyana. Mycologia 94:210–220CrossRefPubMedGoogle Scholar
  72. 72.
    Clement SL, Graves W, Cunningham P, Nebling V, Bounejmate W, Saidi S, Baya B, Chakroun M, Mezni A, Porqueddu C (1997) Acremonium endophytes in Mediterranean tall fescue. In: Bacon CW, Hill NS (eds) Neotyphodium/grass interactions. Springer, New York, pp 49–51CrossRefGoogle Scholar
  73. 73.
    Ghimire SR, Charlton ND, Bell JD, Krishnamurthy YL, Craven KD (2011) Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Divers. 47:19–27. doi: 10.1007/s13225-010-0085-6 CrossRefGoogle Scholar
  74. 74.
    Gond SK, Verma VC, Kumar A, Kharwar RN (2007) Study of endophytic fungal community from different parts of Aegle marmelos Correae (Rutaceae) from Varanasi (India). World J Microb Biot 23:1371–1375CrossRefGoogle Scholar
  75. 75.
    Harman GE (2011) Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol. 189:647–649CrossRefPubMedGoogle Scholar
  76. 76.
    Kusari P, Kusari S, Spiteller M, Kayser O (2013) Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers. 60:137–151. doi: 10.1007/s13225-012-0216-3 CrossRefGoogle Scholar
  77. 77.
    Macia’-Vicente JG, Jansson HB, Mendgen K, Lopez-Llorca LV (2008) Colonization of barley roots by endophytic fungi and their reduction of take-all caused by Gaeumannomyces graminis var. tritici. Can. J. Microbiol. 54:600–609. doi: 10.1139/w08-047 CrossRefGoogle Scholar
  78. 78.
    Nalini MS, Sunayana N, Prakash HS (2014) Endophytic fungal diversity in medicinal plants of Western Ghats, India. International Journal of Biodiversity 9:494213Google Scholar
  79. 79.
    Paparu P, Dubois T, Coyne D, Viljoen A (2009) Dual inoculation of Fusarium oxysporum endophytes in banana: effect on plant colonisation, growth and control of the root burrowing nematode and the banana weevil. Biocontrol Sci Techn 19:639–655CrossRefGoogle Scholar
  80. 80.
    Rosmana A, Samuels GJ, Ismaiel A, Ibrahim ES, Chaverri P, Herawati Y, Asman A (2015) Trichoderma asperellum: a dominant endophyte species in cacao grown in sulawesi with potential for controlling vascular streak dieback disease. Tropical Plant Pathology 40:19–25CrossRefGoogle Scholar
  81. 81.
    Spurr HWJ, Welty RE (1975) Characterization of endophytic fungi in healthy leaves of Nicotiana spp. Phytopathology 65:417–422CrossRefGoogle Scholar
  82. 82.
    Wang B, Priest MJ, Davidson A, Brubaker CL, Woods MJ, Burdon JJ (2007) Fungal endophytes of native Gossypium species in Australia. Mycol. Res. 111:347–354CrossRefPubMedGoogle Scholar
  83. 83.
    Zhou K, Wang W, Peng Y, Yu R, Yue Y, Lai D, Zhou L (2015) Endophytic fungi from Nicotiana tabacum L.and their antibacterial activity. Natural Product Research and Development 27:1847–1852Google Scholar
  84. 84.
    Wilson D (2000) Ecology of woody plant endophytes. Mercel Dekker Inc., New YorkGoogle Scholar
  85. 85.
    McKenna JEJ (2003) An enhanced cluster analysis program with bootstrap significance testing for ecological community analysis. Environ. Model Softw. 18:205–220CrossRefGoogle Scholar
  86. 86.
    Del Olmo RM, Arnold AE (2014) Inter annual variation and host affiliations of endophytic fungi associated with ferns at la Selva, Costa Rica. Mycologia 106:8–21CrossRefGoogle Scholar
  87. 87.
    Higgins KL, Arnold AE, Coley PD, Kursar TK (2014) Communities of fungal endophytes in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecol. 8:1–11CrossRefGoogle Scholar
  88. 88.
    Chobba BI, Elleuch A, Ayadi I, Khannous L, Namsi A, Cerqueira F, Drira N, Gharsallah N, Vallaeys T (2013) Fungal diversity in adult date palm (Phoenix dactylifera L.) revealed by culture-dependent and culture-independent approaches. J Zhejiang Univ Sci B 14:1084–1099CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Khondoker M. G. Dastogeer
    • 1
  • Hua Li
    • 1
  • Krishnapillai Sivasithamparam
    • 1
  • Michael G. K. Jones
    • 1
  • Stephen J. Wylie
    • 1
  1. 1.Plant Biotechnology Group - Plant Virology, Western Australian State Agricultural Biotechnology Centre, School of Veterinary and Life SciencesMurdoch UniversityPerthAustralia

Personalised recommendations