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References

  1. Abdalla MH, El-Tayeb NM. 1981. Preliminary survey of cotton flower mycoflora from Sudan. Trans. Br. Mycol. Soc. 76: 367-370.
    CrossRef
  2. Al-Samarrai TH, Schmid J. 2000. A simple method for extraction of fungal genomic DNA. Lett. Appl. Microbiol. 30:53-56.
    Pubmed CrossRef
  3. Anderson CMT, McGee PA, Nehl DB, Mensah RK. 2007. The fungus Lecanicillium lecanii colonises the plant Gossypium hirsutum and the aphid Aphis gossypii. Australas. Mycol. 26:65-70.
  4. Arnold AE, Maynord J, Gilbert G, Coley PD, Kusar TA. 2000. Are tropical fungal endophytes Hyperdiverse? Ecol. Lett. 3: 267-274.
    CrossRef
  5. Backman PA, Sikora RA. 2008. Endophytes: an emerging tool for biological control. Biol. Control 46: 1-3.
    CrossRef
  6. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, et al. 2006. Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224: 1149-1164.
    Pubmed CrossRef
  7. Bonos SA, Wilson MM, Meyer WA, Funk CR. 2005. Suppression of red thread in fine fescues through endophytemediated resistance. Appl. Turfgrass Sci. 10: 1094-1097.
  8. Brady SF, Clardy J. 2000. CR377, a new pentaketide antifungal agent isolated from an endophytic fungus. J. Nat. Prod. 63:1447-1448.
    CrossRef
  9. Chen J, Zhang LC, Xing YM, Wang YQ, Xing XK, Zhang DW, Guo SX. 2013. Diversity and taxonomy of endophytic Xylariaceous fungi from medicinal plants of Dendrobium (Orchidaceae). PLoS One 8: e58268.
    Pubmed CrossRef
  10. Cortesero AM, Stapel JO, Lewis WJ. 2000. Understanding and manipulating plant attributes to enhance biological control. Biol. Control 17: 35-49.
    CrossRef
  11. Daayf F, Nicole M, Boher B, Pando A, Geiger JP. 1997. Early vascular defense reaction of cotton roots infected with a defoliating mutant strain of Verticillium dahliae. Eur. J. Plant Pathol. 103: 125-136.
    CrossRef
  12. Dennis C, Webster J. 1971. Antagonistic properties of species groups of Trichoderma. Br. Mycol. Soc. 57: 25-39.
    CrossRef
  13. Fahima T, Madi L, Henis Y. 1992. Ultrastructure and germinability of Verticillium dahliae microsclerotia parasitized by Talaromyces flavus on agar medium and in treated soil. Biocontrol Sci. Technol. 2: 69-78.
    CrossRef
  14. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-789.
    CrossRef
  15. Fravel DR, Roberts DP. 1991. In situ evidence for the role of glucose oxidase in the biocontrol of Verticillium wilt by Talaromyces flavus. Biocontrol Sci. Technol. 1: 91-99.
    CrossRef
  16. Fröhlich J, Hyde KD, Petrini O. 2000. Endophytic fungi associated with palms. Mycol. Res. 104: 1202-1212.
    CrossRef
  17. Gamboa MA, Beyman P. 2001. Communities of endophytic fungi in leaves of tropical timber tree Guarea guidonia (Meliaceae). Biotropica 33: 352-360.
    CrossRef
  18. Gasoni L, Gurfinkel D, Stegman B. 1997. The endophyte Cladorrhinum foecundissimum in cotton roots: phosphorus uptake and host growth. Mycol. Res. 101: 867-870.
    CrossRef
  19. Gond SK, Verma VC, Mishra A, Kumar A, Kharwar RN. 2010. Role of fungal endophytes in plant protection. Mycoscience 53: 113-121.
    CrossRef
  20. Gong LJ, Guo SX. 2009. Endophytic fungi from Dracaena cambodiana and Aquilaria sinensis and their antimicrobial activity. Afr. J. Biotechnol. 8: 731-736.
  21. Graner G, Persson P, Meijer J, Alstrom S. 2003. A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol. Lett. 224: 269-276.
    CrossRef
  22. Guo LD, Hyde KD, Liew ECY. 2000. Identification of endophytic fungi from Livistonia chinensis based on morphology and rDNA sequences. New Phytol. 147: 617-630.
    CrossRef
  23. Hata K, Futai K. 1995. Endophytic fungi associated with healthy pine needles and needles infested by the pine needle gall midge, Thecodiplosis japonensis. Can. J. Bot. 73: 384-390.
    CrossRef
  24. James C. 2002. Global Review of Commercialized Transgenic Crops: 2001 Feature: Bt Cotton. ISAAA Briefs 26.
  25. Kharwar RN, Maurya AL, Verma VC, Kumar A, Gond SK, Mishra A. 2012. Diversity and antimicrobial activity of endophytic fungal community isolated from medicinal plant Cinnamomum camphora. Proc. Nat. Acad. Sci. India B Biol. Sci. 82: 557-565.
  26. Kharw ar RN, V erma V C, K umar A, Gond S K, H arper JK, Hess WM, et al. 2009. Javanicin, an antibacterial naphthaquinone from an endophytic fungus of Neem, Chloridium sp. Curr. Microbiol. 58: 233-238.
  27. Kharwar RN, Verma VC, Strobel G, Ezra D. 2008. The endophytic fungal complex of Catharanthus roseus (L. G. Don). Curr. Sci. 95: 228-233.
  28. Kim KK, Fravel DR, Papavizas GC. 1998. Identification of a metabolite produced by Talaromyces flavus as glucose oxidase and its role in the biocontrol of Verticillium dahliae. Phytopathology 78: 25-29.
  29. Kumaresan V, Suryanarayanan TS. 2001. Occurrence and distribution of endophytic fungi in a mangrove community. Mycol. Res. 105: 1388-1391.
    CrossRef
  30. Lacap DC, Hyde KD, Liew ECY. 2003. An evaluation of the fungal ‘morphotype’ concept based on ribosomal DNA sequences. Fungal Divers. 12: 53-66.
  31. Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, Döhlemann S, Zuccaro A. 2013. Host-related metabolic cues affect colonization strategies of a root endophyte. Proc. Nat. Acad. Sci. 110: 13965-13970.
    Pubmed CrossRef
  32. 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.
    CrossRef
  33. Larena I, Sabuquillo P, Melgarejo P, De Cal A. 2003. Biocontrol of Fusarium and Verticillium wilt of tomato by Penicillium oxalicum under greenhouse and field conditions. J. Phytopathol. 151: 507-512.
    CrossRef
  34. Lindner DL, Carlsen T, Henrik Nilsson R, Davey M, Schumacher T, Kauserud H. 2013. Employing 454 amplicon pyrosequencing to reveal intragenomic divergence in the internal transcribed spacer rDNA region in fungi. Ecol. Evol. DOI: 10.1002/ece3.586.
    CrossRef
  35. Linnakoski R, Puhakka-Tarvainen H, Pappinen A. 2012. Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecol. 5: 298-308.
    CrossRef
  36. Mejía LC, Rojas EI, Maynard Z, Bael SV, Arnold AE, Hebbar H, et al. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol. Control 46: 4-14.
    CrossRef
  37. Mitter B, Petric ASG, Chain P, Trognitz F, Nowak J, Compant S, Sessitsch A. 2013. Genome analysis, ecology, and plant growth promotion of the endophyte Burkholderia phytofirmans strain PsJN. Mol. Microb. Ecol. Rhizos. 1: 865874.
  38. Naraghi L, Heydari A, Rezaee S, Razavi M, Afshari-Azad H. 2010. Biological control of Verticillium wilt of greenhouse cucumber by Talaromyces flavus. Phytopathol. Mediterranea 49:321-329.
  39. Petrini O. 1991. Fungal endophytes of tree leaves, pp 179-197. In Andrews JA, Hirano SS (eds.). Microbial Ecology of Leaves. Springer, New York.
    CrossRef
  40. Rúa MA, McCulley RL, Mitchell CE. 2013. Fungal endophyte infection and host genetic background jointly modulate host response to an aphid-transmitted viral pathogen. J. Ecol. 101: 1007-1018.
    CrossRef
  41. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  42. Schnathorst WC. 1981. Life cycle and epidemiology of Verticillium, pp. 81-111. In Mace ME, Bell AA, Beckman CH (eds.). Fungal Wilt Disease of Plants. Academic Press, New York.
    CrossRef
  43. Sikora RA, Schäfer K, Dababat AA. 2007. Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas. Plant Pathol. 36: 124134.
    CrossRef
  44. Simpson EH. 1951. The interpretation of interaction in contingency tables. J. R. Stat. Soc. B 13: 238-241.
  45. Strobel GA. 2003. Endophytes as sources of bioactive products. Microbes Infect. 5: 535-544.
    CrossRef
  46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
    Pubmed CrossRef
  47. Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, et al. 2010. Fungal endophyte diversity in coffee plants from Colombia, Hawai’i, Mexico and Puerto Rico. Fungal Ecol. 3: 122-138.
    CrossRef
  48. Verma V C, G ond SK, Kumar A, K harw ar R N, S trobel G . 2007. The endophytic mycoflora of bark, leaf, and stem tissues of Azadirachta indica A. Juss (neem) from Varanasi (India). Microb. Ecol. 54: 119-125.
    Pubmed CrossRef
  49. Verma V C, Kharw ar RN, S trobel GA. 2009. C hemical and functional diversity of natural products from plant associated endophytic fungi. Nat. Prod. Commun. 4: 1511-1532.
    Pubmed
  50. Vieira PDS, Motta CMS, Lima D, Torres JB, Quecine MC, Azevedo JL, Oliveira NTD. 2011. Endophytic fungi associated with transgenic and non-transgenic cotton. Mycology 2: 91-97.
    CrossRef
  51. Wang B, Priest MJ, Davidson A, Brubaker CL, Woods MJ, Burdon JJ. 2007. Fungal endophytes of native Gossypium species in Australia. Mycol. Res. 111: 347-354.
    Pubmed CrossRef
  52. Whipps JM. 1997. Developments in the biological control of soilborne plant pathogens. Adv. Bot. Res. 26: 1-134.
    CrossRef
  53. Whipps JM, Magan N. 1987. Effects of nutrient status and water potential of media on fungal growth and antagonistpathogen interactions. EPPO Bulletin 17: 581-591.
    CrossRef
  54. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Genet. Evol. 38: 315-322.
  55. Wilson D. 1995. Endophyte: the evolution of a term and clarification of its use and definition. Oikos 73: 274-276.
    CrossRef
  56. Xia Z, Achar PN, Gu B. 1998. Vegetative compatibility groupings of Verticillium dahliae from cotton in mainland China. Eur. J. Plant Pathol. 104: 871-876.
    CrossRef
  57. Zhang J, Howell CR, Starr JL, Wheeler MH. 1996. Frequency of isolation and the pathogenicity of Fusarium species associated with roots of healthy cotton seedlings. Mycol. Res. 100: 747752.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(9): 1149-1161

Published online September 28, 2014 https://doi.org/10.4014/jmb.1402.02035

Copyright © The Korean Society for Microbiology and Biotechnology.

Diversity of Endophytic Fungi from Different Verticillium-Wilt-Resistant Gossypium hirsutum and Evaluation of Antifungal Activity Against Verticillium dahliae In Vitro

Zhi-Fang Li 1, Ling-Fei Wang 1, Zi-Li Feng 1, Li-Hong Zhao 1, Yong-Qiang Shi 1 and He-Qin Zhu 1*

State Key Laboratory of Cotton Biology, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang, Henan 455000, P. R. China

Received: February 18, 2014; Accepted: May 16, 2014

Abstract

Cotton plants were sampled and ranked according to their resistance to Verticillium wilt. In
total, 642 endophytic fungi isolates representing 27 genera were recovered from Gossypium
hirsutum root, stem, and leaf tissues, but were not uniformly distributed. More endophytic
fungi appeared in the leaf (391) compared with the root (140) and stem (111) sections.
However, no significant difference in the abundance of isolated endophytes was found among
resistant cotton varieties. Alternaria exhibited the highest colonization frequency (7.9%),
followed by Acremonium (6.6%) and Penicillium (4.8%). Unlike tolerant varieties, resistant and
susceptible ones had similar endophytic fungal population compositions. In three
Verticillium-wilt-resistant cotton varieties, fungal endophytes from the genus Alternaria were
most frequently isolated, followed by Gibberella and Penicillium. The maximum concentration
of dominant endophytic fungi was observed in leaf tissues (0.1797). The evenness of stem
tissue endophytic communities (0.702) was comparatively more uniform than the other two
tissues. Eighty endophytic fungi selected from 27 genera were evaluated for their inhibition
activity against highly virulent Verticillium dahliae isolate Vd080 in vitro. Thirty-nine isolates
exhibited fungistasis against the pathogen at varying degrees. Seven species, having high
growth inhibition rates (≥75%), exhibited strong antifungal activity against V. dahliae. The
antifungal activity of both volatile and nonvolatile metabolites was also investigated. The
nonvolatile substances produced by CEF-818 (Penicillium simplicissimum), CEF-325 (Fusarium
solani), CEF-714 (Leptosphaeria sp.), and CEF-642 (Talaromyces flavus) completely inhibited V.
dahliae growth. These findings deepen our understanding of cotton-endophyte interactions
and provide a platform for screening G. hirsutum endophytes with biocontrol potential.

Keywords: cotton, Endophytic fungi, V. dahliae, Verticillium wilt, Biological control

References

  1. Abdalla MH, El-Tayeb NM. 1981. Preliminary survey of cotton flower mycoflora from Sudan. Trans. Br. Mycol. Soc. 76: 367-370.
    CrossRef
  2. Al-Samarrai TH, Schmid J. 2000. A simple method for extraction of fungal genomic DNA. Lett. Appl. Microbiol. 30:53-56.
    Pubmed CrossRef
  3. Anderson CMT, McGee PA, Nehl DB, Mensah RK. 2007. The fungus Lecanicillium lecanii colonises the plant Gossypium hirsutum and the aphid Aphis gossypii. Australas. Mycol. 26:65-70.
  4. Arnold AE, Maynord J, Gilbert G, Coley PD, Kusar TA. 2000. Are tropical fungal endophytes Hyperdiverse? Ecol. Lett. 3: 267-274.
    CrossRef
  5. Backman PA, Sikora RA. 2008. Endophytes: an emerging tool for biological control. Biol. Control 46: 1-3.
    CrossRef
  6. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, et al. 2006. Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224: 1149-1164.
    Pubmed CrossRef
  7. Bonos SA, Wilson MM, Meyer WA, Funk CR. 2005. Suppression of red thread in fine fescues through endophytemediated resistance. Appl. Turfgrass Sci. 10: 1094-1097.
  8. Brady SF, Clardy J. 2000. CR377, a new pentaketide antifungal agent isolated from an endophytic fungus. J. Nat. Prod. 63:1447-1448.
    CrossRef
  9. Chen J, Zhang LC, Xing YM, Wang YQ, Xing XK, Zhang DW, Guo SX. 2013. Diversity and taxonomy of endophytic Xylariaceous fungi from medicinal plants of Dendrobium (Orchidaceae). PLoS One 8: e58268.
    Pubmed CrossRef
  10. Cortesero AM, Stapel JO, Lewis WJ. 2000. Understanding and manipulating plant attributes to enhance biological control. Biol. Control 17: 35-49.
    CrossRef
  11. Daayf F, Nicole M, Boher B, Pando A, Geiger JP. 1997. Early vascular defense reaction of cotton roots infected with a defoliating mutant strain of Verticillium dahliae. Eur. J. Plant Pathol. 103: 125-136.
    CrossRef
  12. Dennis C, Webster J. 1971. Antagonistic properties of species groups of Trichoderma. Br. Mycol. Soc. 57: 25-39.
    CrossRef
  13. Fahima T, Madi L, Henis Y. 1992. Ultrastructure and germinability of Verticillium dahliae microsclerotia parasitized by Talaromyces flavus on agar medium and in treated soil. Biocontrol Sci. Technol. 2: 69-78.
    CrossRef
  14. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-789.
    CrossRef
  15. Fravel DR, Roberts DP. 1991. In situ evidence for the role of glucose oxidase in the biocontrol of Verticillium wilt by Talaromyces flavus. Biocontrol Sci. Technol. 1: 91-99.
    CrossRef
  16. Fröhlich J, Hyde KD, Petrini O. 2000. Endophytic fungi associated with palms. Mycol. Res. 104: 1202-1212.
    CrossRef
  17. Gamboa MA, Beyman P. 2001. Communities of endophytic fungi in leaves of tropical timber tree Guarea guidonia (Meliaceae). Biotropica 33: 352-360.
    CrossRef
  18. Gasoni L, Gurfinkel D, Stegman B. 1997. The endophyte Cladorrhinum foecundissimum in cotton roots: phosphorus uptake and host growth. Mycol. Res. 101: 867-870.
    CrossRef
  19. Gond SK, Verma VC, Mishra A, Kumar A, Kharwar RN. 2010. Role of fungal endophytes in plant protection. Mycoscience 53: 113-121.
    CrossRef
  20. Gong LJ, Guo SX. 2009. Endophytic fungi from Dracaena cambodiana and Aquilaria sinensis and their antimicrobial activity. Afr. J. Biotechnol. 8: 731-736.
  21. Graner G, Persson P, Meijer J, Alstrom S. 2003. A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol. Lett. 224: 269-276.
    CrossRef
  22. Guo LD, Hyde KD, Liew ECY. 2000. Identification of endophytic fungi from Livistonia chinensis based on morphology and rDNA sequences. New Phytol. 147: 617-630.
    CrossRef
  23. Hata K, Futai K. 1995. Endophytic fungi associated with healthy pine needles and needles infested by the pine needle gall midge, Thecodiplosis japonensis. Can. J. Bot. 73: 384-390.
    CrossRef
  24. James C. 2002. Global Review of Commercialized Transgenic Crops: 2001 Feature: Bt Cotton. ISAAA Briefs 26.
  25. Kharwar RN, Maurya AL, Verma VC, Kumar A, Gond SK, Mishra A. 2012. Diversity and antimicrobial activity of endophytic fungal community isolated from medicinal plant Cinnamomum camphora. Proc. Nat. Acad. Sci. India B Biol. Sci. 82: 557-565.
  26. Kharw ar RN, V erma V C, K umar A, Gond S K, H arper JK, Hess WM, et al. 2009. Javanicin, an antibacterial naphthaquinone from an endophytic fungus of Neem, Chloridium sp. Curr. Microbiol. 58: 233-238.
  27. Kharwar RN, Verma VC, Strobel G, Ezra D. 2008. The endophytic fungal complex of Catharanthus roseus (L. G. Don). Curr. Sci. 95: 228-233.
  28. Kim KK, Fravel DR, Papavizas GC. 1998. Identification of a metabolite produced by Talaromyces flavus as glucose oxidase and its role in the biocontrol of Verticillium dahliae. Phytopathology 78: 25-29.
  29. Kumaresan V, Suryanarayanan TS. 2001. Occurrence and distribution of endophytic fungi in a mangrove community. Mycol. Res. 105: 1388-1391.
    CrossRef
  30. Lacap DC, Hyde KD, Liew ECY. 2003. An evaluation of the fungal ‘morphotype’ concept based on ribosomal DNA sequences. Fungal Divers. 12: 53-66.
  31. Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, Döhlemann S, Zuccaro A. 2013. Host-related metabolic cues affect colonization strategies of a root endophyte. Proc. Nat. Acad. Sci. 110: 13965-13970.
    Pubmed CrossRef
  32. 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.
    CrossRef
  33. Larena I, Sabuquillo P, Melgarejo P, De Cal A. 2003. Biocontrol of Fusarium and Verticillium wilt of tomato by Penicillium oxalicum under greenhouse and field conditions. J. Phytopathol. 151: 507-512.
    CrossRef
  34. Lindner DL, Carlsen T, Henrik Nilsson R, Davey M, Schumacher T, Kauserud H. 2013. Employing 454 amplicon pyrosequencing to reveal intragenomic divergence in the internal transcribed spacer rDNA region in fungi. Ecol. Evol. DOI: 10.1002/ece3.586.
    CrossRef
  35. Linnakoski R, Puhakka-Tarvainen H, Pappinen A. 2012. Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecol. 5: 298-308.
    CrossRef
  36. Mejía LC, Rojas EI, Maynard Z, Bael SV, Arnold AE, Hebbar H, et al. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol. Control 46: 4-14.
    CrossRef
  37. Mitter B, Petric ASG, Chain P, Trognitz F, Nowak J, Compant S, Sessitsch A. 2013. Genome analysis, ecology, and plant growth promotion of the endophyte Burkholderia phytofirmans strain PsJN. Mol. Microb. Ecol. Rhizos. 1: 865874.
  38. Naraghi L, Heydari A, Rezaee S, Razavi M, Afshari-Azad H. 2010. Biological control of Verticillium wilt of greenhouse cucumber by Talaromyces flavus. Phytopathol. Mediterranea 49:321-329.
  39. Petrini O. 1991. Fungal endophytes of tree leaves, pp 179-197. In Andrews JA, Hirano SS (eds.). Microbial Ecology of Leaves. Springer, New York.
    CrossRef
  40. Rúa MA, McCulley RL, Mitchell CE. 2013. Fungal endophyte infection and host genetic background jointly modulate host response to an aphid-transmitted viral pathogen. J. Ecol. 101: 1007-1018.
    CrossRef
  41. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
    Pubmed
  42. Schnathorst WC. 1981. Life cycle and epidemiology of Verticillium, pp. 81-111. In Mace ME, Bell AA, Beckman CH (eds.). Fungal Wilt Disease of Plants. Academic Press, New York.
    CrossRef
  43. Sikora RA, Schäfer K, Dababat AA. 2007. Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas. Plant Pathol. 36: 124134.
    CrossRef
  44. Simpson EH. 1951. The interpretation of interaction in contingency tables. J. R. Stat. Soc. B 13: 238-241.
  45. Strobel GA. 2003. Endophytes as sources of bioactive products. Microbes Infect. 5: 535-544.
    CrossRef
  46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
    Pubmed CrossRef
  47. Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, et al. 2010. Fungal endophyte diversity in coffee plants from Colombia, Hawai’i, Mexico and Puerto Rico. Fungal Ecol. 3: 122-138.
    CrossRef
  48. Verma V C, G ond SK, Kumar A, K harw ar R N, S trobel G . 2007. The endophytic mycoflora of bark, leaf, and stem tissues of Azadirachta indica A. Juss (neem) from Varanasi (India). Microb. Ecol. 54: 119-125.
    Pubmed CrossRef
  49. Verma V C, Kharw ar RN, S trobel GA. 2009. C hemical and functional diversity of natural products from plant associated endophytic fungi. Nat. Prod. Commun. 4: 1511-1532.
    Pubmed
  50. Vieira PDS, Motta CMS, Lima D, Torres JB, Quecine MC, Azevedo JL, Oliveira NTD. 2011. Endophytic fungi associated with transgenic and non-transgenic cotton. Mycology 2: 91-97.
    CrossRef
  51. Wang B, Priest MJ, Davidson A, Brubaker CL, Woods MJ, Burdon JJ. 2007. Fungal endophytes of native Gossypium species in Australia. Mycol. Res. 111: 347-354.
    Pubmed CrossRef
  52. Whipps JM. 1997. Developments in the biological control of soilborne plant pathogens. Adv. Bot. Res. 26: 1-134.
    CrossRef
  53. Whipps JM, Magan N. 1987. Effects of nutrient status and water potential of media on fungal growth and antagonistpathogen interactions. EPPO Bulletin 17: 581-591.
    CrossRef
  54. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Genet. Evol. 38: 315-322.
  55. Wilson D. 1995. Endophyte: the evolution of a term and clarification of its use and definition. Oikos 73: 274-276.
    CrossRef
  56. Xia Z, Achar PN, Gu B. 1998. Vegetative compatibility groupings of Verticillium dahliae from cotton in mainland China. Eur. J. Plant Pathol. 104: 871-876.
    CrossRef
  57. Zhang J, Howell CR, Starr JL, Wheeler MH. 1996. Frequency of isolation and the pathogenicity of Fusarium species associated with roots of healthy cotton seedlings. Mycol. Res. 100: 747752.
    CrossRef