Skip to main content
Log in

A Phylogenetic Evaluation of Whether Endophytes Become Saprotrophs at Host Senescence

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Fungal endophytes and saprotrophs generally play an important ecological role within plant tissues and dead plant material. Several reports based solely on morphological observations have postulated that there is an intimate link between endophytes and saprotrophs. This study aims to provide valuable insight as to whether some endophytic fungi manifest themselves as saprotrophs upon host decay. Ribosomal DNA-based sequence comparison and phylogenetic relationships from 99 fungal isolates (endophytes, mycelia sterilia, and saprotrophs) recovered from leaves and twigs of Magnolia liliifera were investigated in this study. Molecular data suggest there are fungal taxa that possibly exist as endophytes and saprotrophs. Isolates of Colletotrichum, Fusarium, Guignardia, and Phomopsis, which are common plant endophytes, have high sequence similarity and are phylogenetically related to their saprotrophic counterparts. This provides evidence to suggest that some endophytic species change their ecological strategies and adopt a saprotrophic lifestyle. The implication of these findings on fungal biodiversity and host specificity is also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Arnold, AE, Maynard, Z, Gilbert, GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105: 1502–1507

    Google Scholar 

  2. Arnold, AE, Maynard, Z, Gilbert, GS, Coley, PD, Kursar, TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3: 267–274

    Article  Google Scholar 

  3. Arnold, AE, Mejía, LC, Kyllo, D, Rojas, EI, Maynard, Z, Robbins, N, Herre, EA (2003) Fungal endophytes limit pathogen in a tropical tree. Proc Natl Acad Sci 100: 15649–15654

    Article  PubMed  CAS  Google Scholar 

  4. Baayen, RP, Bonants, PJM, Verkley, G, Carroll, GC, van der Aa, HA, de Weerdt, M, van Brouwershaven, IR, Schutte, GC, Maccheroni, W Jr, Glienke de Blanco, C, Azevedo, JL (2002) Nonpathogenic isolates of the citrus black spot fungus, Guignardia citricarpa, identified as a cosmopolitan endophyte of woody plants, G. mangiferae (Phyllosticta capitalensis). Phytopathology 92: 464–477

    Article  PubMed  CAS  Google Scholar 

  5. Bacon, CW, White, JF (1994) Biotechnology of Endophytic Fungi of Grasses. CRC Press, Boca Raton, FL

    Google Scholar 

  6. Bayman, P, Lebrón, LL, Tremblay, RL, Lodges, DJ (1997) Variation in endophytic fungi from roots and leaves of Lepanthes (Orchidaceae). New Phytol 135: 143–149

    Article  Google Scholar 

  7. Bayman, P, Angulo-Sandoval, P, Báez-Ortiz, Z, Lodge, DJ (1998) Distribution and dispersal of Xylaria endophytes in two tree species in Puerto Rico. Mycol Res 102: 944–948

    Article  Google Scholar 

  8. Benhamou, N, Garand, C, Goulet, A (2002) Ability of nonpathogenic Fusarium oxysporum strain Fo47 to induce resistance against Pythium ulimum infection in cucumber. Appl Environ Microbiol 68: 4044–4060

    Article  PubMed  CAS  Google Scholar 

  9. Bills, GF (1996) Isolation and analysis of endophytic fungal communities from woody plants. In: Redlin, SC, Carris, LM (Eds.) Endophytic Fungi in Grasses and Woody Plants. APS Press, St. Paul, MN, pp 31–65

    Google Scholar 

  10. Brown, KB, Hyde, KD, Guest, DI (1998) Preliminary studies on endophytic fungal communities of Musa acuminata species complex in Hong Kong and Australia. Fungal Divers 1: 27–51

    Google Scholar 

  11. Bussaban, B, Lumyong, S, Lumyong, P, McKenzie, EHC, Hyde, KD (2001) Endophytic fungi from Amomum siamense. Can J Microbiol 47: 943–948

    Article  PubMed  CAS  Google Scholar 

  12. Cai, L, Jeewon, R, Hyde, KD (2005) Phylogenetic evaluation and taxonomic revision of Schizothecium based on ribosomal DNA and protein coding genes. Fungal Divers 19: 1–21

    CAS  Google Scholar 

  13. Cannon, PF (1997) Strategies for rapid assessment of fungal diversity. Biodivers Conserv 6: 669–680

    Article  Google Scholar 

  14. Cannon, PF, Simmons, CM (2002) Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve. Mycologia 94: 210–220

    Article  Google Scholar 

  15. Carroll, G (1995) Forest endophytes: pattern and process. Can J Bot 73: 1316–1324

    Google Scholar 

  16. Clay, K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69: 10–16

    Article  Google Scholar 

  17. Davis, EC, Franklin, JB, Shaw, AJ, Vilgalys, R (2003) Endophytic Xylaria (Xylariaceae) among liverworts and angiosperms: phylogenetics, distribution, and symbiosis. Am J Bot 90: 1661–1667

    Google Scholar 

  18. De Bary, A (1866) Morpholodie und Physiologie del Pilze. Flechten und Myxomyceten. Engelmann, Leipzig, Germany

    Google Scholar 

  19. Dickinson, CH (1976) Fungi on the aerial surface of higher plants. In: Preece, TF, Dickinson, CH (Eds.) Microbiology of Aerial Plant Surfaces. Academic Press, London, pp 293–324

    Google Scholar 

  20. Fröhlich, J, Hyde, KD (1999) Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodivers Conserv 8: 977–1004

    Article  Google Scholar 

  21. Fröhlich, J, Hyde, KD, Petrini, O (2000) Endophytic fungi associated with palms. Mycol Res 104: 1202–1212

    Article  Google Scholar 

  22. Gamboa, MA, Bayman, P (2001) Communities of endophytic fungi in leaves of a tropical timber tree (Guarea guidonia: Meliaceae). Biotropica 33: 352–360

    Google Scholar 

  23. Ganley, RJ, Brunsfeld, SJ, Newcombe, G (2004) A community of unknown, endophytic fungi in western white pine. Proc Natl Acad Sci 101: 10107–10112

    Article  PubMed  CAS  Google Scholar 

  24. Ghimire, SR, Hyde, KD (2004) Fungal endophytes. In: Varma, A, Abbott, L, Werner, D, Hampp, R (Eds.) Plant Surface Microbiology. Springer-Verlag, Berlin, pp 281–292

    Google Scholar 

  25. Guo, LD, Huang, GR, Wang, Y, He, WH, Zheng, WH, Hyde, KD (2003) Molecular identification of white morphotype strains of endophytic fungi from Pinus tabulaeformis. Mycol Res 107: 680–688

    Article  PubMed  CAS  Google Scholar 

  26. Guo, LD, Hyde, KD, Liew, ECY (2000) Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 147: 617–630

    Article  CAS  Google Scholar 

  27. Guo, LD, Hyde, KD, Liew, ECY (2001) Detection and taxonomic placement of endophytic fungi within frond tissues of Livistona chinensis based on rDNA sequences. Mol Phylogen Evol 19: 1–13

    Article  CAS  Google Scholar 

  28. Hawksworth, DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95: 641–655

    Google Scholar 

  29. Hawksworth, DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105: 1422–1432

    Google Scholar 

  30. Hawksworth, DL (2003) Monitoring and safeguarding fungal resources worldwide: the need for an international collaborative MycoAction plan. Fungal Divers 13: 13–27

    Google Scholar 

  31. Hennequin, C, Abachin, E, Symoens, F, Lavarde, V, Reboux, G, Nolard, N, Berche, P (1999) Identification of Fusarium species involved in human infections by 28S rRNA gene sequencing. J Clin Microbiol 37: 3586–3589

    PubMed  CAS  Google Scholar 

  32. Howlett, BJ (2004) Current knowledge of the interaction between Brassica napus and Leptosphaeria maculans. Can J Plant Pathol/Rev Can Phytopathol 26: 245–252

    Google Scholar 

  33. Huelsenbeck, PJ, Ronquist, FR (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755

    Article  PubMed  CAS  Google Scholar 

  34. Hyde, KD (1995) Fungi from palms. XX. The genus Guignardia. Sydowia 47: 180–198

    Google Scholar 

  35. Hyde, KD (2001) Where are the missing fungi? Does Hong Kong have the answers? Mycol Res 105: 1514–1518

    Google Scholar 

  36. Hyde, KD, Bussaban, B, Paulus, B, Crous, PW, Lee, S, Mckenzie, EHC, Photita, W, Lumyong, S (2006) Biodiversity of saprobic fungi. Biodivers Conserv (in press).

  37. Hyde, KD, Zhou, DQ, Dalisay, TE (2002) Bambusicolous fungi: a review. Fungal Divers 9: 1–14

    Google Scholar 

  38. Hyde, KD, Zhou, DQ, McKenzie, EHC, Ho, WH, Dalisay, T (2002) Vertical distribution of saprobic fungi on bamboo culms. Fungal Divers 11: 109–118

    Google Scholar 

  39. Jeewon, R, Cai, L, Liew, ECY, Zhang, KQ, Hyde, KD (2003) Dyrithiopsis lakefuxianensis gen. et sp. nov from Fuxian Lake, Yunnan, China, and notes on the taxonomic confusing surrounding Dyrithium. Mycologia 95: 911–920

    Article  Google Scholar 

  40. Jeewon, R, Liew, ECY, Hyde, KD (2004) Phylogenetic evaluation of species nomenclature of Pestalotiopsis in relation to host association. Fungal Divers 17: 39–55

    Google Scholar 

  41. Kerényi, Z, Moretti, A, Waalwijk, C, Oláh, B, Hornok, L (2004) Mating type sequences in asexually reproducing Fusarium species. Appl Environ Microbiol 70: 4419–4423

    Article  PubMed  CAS  Google Scholar 

  42. Kumar, DSS, Hyde, KD (2004) Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Divers 17: 69–90

    CAS  Google Scholar 

  43. Kuo, KC, Hoch, HC (1996) The parasitic relationship between Phyllosticta ampelicida and Vitis vinifera. Mycologia 88: 626–634

    Article  Google Scholar 

  44. Lacap, DC, Hyde, KD, Liew, ECY (2003) An evaluation of the fungal ‘morphotype’ concept on ribosomal DNA sequence. Fungal Divers 12: 53–66

    Google Scholar 

  45. Lee, S, Mel'nik, V, Taylor, JE, Crous, PW (2004) Diversity of saprobic hyphomycetes on Proteacae and Restionaceae from South Africa. Fungal Divers 17: 91–114

    Google Scholar 

  46. Lee, S, Roets, F, Crous, PW (2005) Protea infructescences represent a unique fungal niche. Fungal Divers 19: 69–78

    Google Scholar 

  47. Lumyong, S, Lumyong, P, Hyde, KD (2004) Endophytes. In: Jones, EBG, Tanticharoen, M, Hyde, KD (Eds.) Thai Fungal Diversity. BIOTEC, Thailand, pp 197–205

    Google Scholar 

  48. McKenzie, EHC, Whitton, SR, Hyde, KD (2002) The Pandanaceae—does it have a diverse and unique fungal biota? In: Watling, R, Franklin, JC, Ainsuorth, AM, Isaac, S, Robinson, CH (Eds.) Tropical Mycology, vol. 2, Micromycota. CAB International, Wallingford, UK, pp 51–61

    Google Scholar 

  49. Meyer, L, Slippers, B, Korsten, L, Kotzé, JM, Wingfield, MJ (2001) Two distinct Guignardia species associated with citrus in South Africa. S Afr J Sci 97: 191–194

    CAS  Google Scholar 

  50. Nirenberg, HI, Samuels, GJ (2000) Nectria and Fusarium. II. Cosmospora zealandica comb. nov. and its anamorph, Fusarium zealandicum sp. nov. Can J Bot 78: 1482–1487

    Article  Google Scholar 

  51. Nylander, JAA (2004) MrModeltest 2.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  52. Okane, I, Lumyong, S, Nakagiri, A (2003) Extensive host range of an endophytic fungus, Guignardia endophyllicola (anamorph: Phyllosticta capitalensis). Mycoscience 44: 353–363

    Article  Google Scholar 

  53. Okane, I, Nakagiri, A, Ito, T (2001) Identity of Guignardia sp. inhabiting ericaceous plants. Can J Bot 79: 101–109

    Article  Google Scholar 

  54. Pereira, JO, Azevedo, JL, Petrini, O (1993) Endophytic fungi of Stylosanthes: a first report. Mycologia 85: 362–364

    Article  Google Scholar 

  55. Petrini, O (1991) Fungal endophytes of tree leaves. In: Andrew, JH, Hirano, SS (Eds.) Microbial Ecology of Leaves. Springer-Verlag, New York, pp 179–197

    Google Scholar 

  56. Petrini, O (1996) Ecological and physiological aspects of host specific in endophytic fungi. In: Redlin, SC, Carris, LM (Eds.) Endophytic Fungi in Grasses and Woody Plants 9. APS Press, St. Paul, MN, pp 87–100

    Google Scholar 

  57. 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: 233–238

    Article  Google Scholar 

  58. Petrini, O, Petrini, LE, Rodrigues, K (1995) Xylariaceaous endophytes: an exercise in biodiversity. Fitopatol Bras 20: 531–539

    Google Scholar 

  59. Petrini, O, Sieber, TH, Toti, L, Viret, O (1992) Ecology, metabolite production and substrate utilization in endophytic fungi. Nat Toxins 1: 185–196

    Article  PubMed  CAS  Google Scholar 

  60. Photita, W, Lumyong, S, Lumyong, P, Ho, WH, McKenzie, EHC, Hyde, KD (2001) Fungi on Musa acuminata in Hong Kong. Fungal Divers 6: 99–106

    Google Scholar 

  61. Photita, W, Lumyong, S, Lumyong, P, McKenzie, EHC, Hyde, KD (2001) Endophytic fungi of wild banana (Musa acuminata) at Doi Suthep-Pui National park, in Thailand. Mycol Res 105: 1508–1513

    Google Scholar 

  62. Photita, W, Lumyong, S, Lumyong, P, McKenzie, EHC, Hyde, KD (2004) Are some endophytes from Musa acuminata latent pathogens? Fungal Divers 16: 131–140

    Google Scholar 

  63. Pointing, SB, Parungao, MM, Hyde, KD (2003) Production of wood-decay enzymes, mass loss and lignin solubilization in wood by tropical Xylariaceae. Mycol Res 107: 231–235

    Article  PubMed  CAS  Google Scholar 

  64. Promputtha, I, Jeewon, R, Lumyong, S, McKenzie, EHC, Hyde, KD (2005) Ribosomal DNA fingerprinting in the identification of nonsporulating endophytes from Magnolia liliifera (Magnoliaceae). Fungal Divers 20: 167–186

    Google Scholar 

  65. Promputtha, I, Lymyong, S, Lumyong, P, McKenzie, EHC, Hyde, KD (2002) Fungal succession of senescent leaves of Manglietia garrettii in Doi Suthep-Pui National Park, northern Thailand. Fungal Divers 10: 89–100

    Google Scholar 

  66. Promputtha, I, Lumyong, S, Lumyong, P, McKenzie, EHC, Hyde, KD (2004) Fungal saprobes on dead leaves of Magnolia liliifera (Magnoliaceae) in Thailand. Cryptogamie Mycol 25: 315–321

    Google Scholar 

  67. Rajagopalan, C (1996) Studies on four species of wood rotting fungi. Trans Kans Acad Sci 68: 541–552

    Google Scholar 

  68. Rodrigues, KF, Sieber, TN, Grünig, CR, Holdenrieder, O (2004) Characterization of Guignardia mangiferae isolated from tropical plants based on morphology ISSR-PCR amplifications and ITS1–5.8S–ITS2 sequences. Mycol Res 108: 45–52

    Article  PubMed  CAS  Google Scholar 

  69. Rogers, JD (2000) Thoughts and musings on tropical Xylariaceae. Mycol Res 104: 1412–1420

    Article  Google Scholar 

  70. Rubini, MR, Silva-Ribeiro, RT, Pomella, AWV, Maki, CS, Araújo, WL, dos Santos, DR, Azevedo, JL (2005) Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches' Broom Disease. Int J Biol Sci 1: 24–33

    PubMed  CAS  Google Scholar 

  71. Saikkonen, K, Faeth, SH, Helander, M, Sullivan, TJ (1998) Fungal Endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29: 319–343

    Article  Google Scholar 

  72. Shearer, JF (2001) Recovery of endophytic fungi from Myriophyllum spicatum. Tech Note, U.S. Army Eng. Waterways Exp. Sta., Vicksburg, MS

  73. Sivanesan, A (1996) Corynesporasca caryotae gen. et sp. nov. with a Corynespora anamorph, and the family Corynesporascaceae. Mycol Res 100: 783–788

    Google Scholar 

  74. Southcott, KA, Johnson, JA (1997) Isolation of endophytes from two species of palm from Bermuda. Can J Microbiol 43: 789–792

    Article  CAS  Google Scholar 

  75. Stone, JK, Bacon, CW, White, JE (2000) An overview of endophytic microbes: endophytism defined. In: Bacon, CW, White, JF (Eds.) Microbial endophytes. Marcel Dekker, New York, pp 3–29

    Google Scholar 

  76. Summerbell, RC, Schroers, HJ (2002) Analysis of phylogenetic relationship of Cylindrocarpon lichenicola and Acremonium falciforme to the Fusarium solani species complex and a review of similarities in the spectrum of opportunistic infections caused by these fungi. J Clin Microbiol 40: 2866–2875

    Article  PubMed  CAS  Google Scholar 

  77. Suryanarayanan, TS, Murali, TS, Venkatesan, G (2002) Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Can J Bot 80: 818–826

    Article  Google Scholar 

  78. Suryanarayanan, TS, Venkatesan, G, Murali, TS (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci 85: 489–493

    Google Scholar 

  79. Suryanarayanan, TS, Vijaykrishna, D (2001) Fungal endophytes of aerial roots of Ficus benghalensis. Fungal Divers 8: 155–161

    Google Scholar 

  80. Swofford, DL (2002) PAUP*. Phylogenetis Analysis Using Parsimony (*and Other Methods), version 4.0b10 edn. Sinauer Associates, Sunderland, MA

  81. Tomita, F (2003) Endophytes in Southeast Asia and Japan: their taxonomic diversity and potential applications. Fungal Divers 14: 187–204

    Google Scholar 

  82. Urairuj, C, Kanongnuch, C, Lumyong, S (2003) Lignolytic enzymes from tropical endophytic Xylariaceae. Fungal Divers 13: 209–219

    Google Scholar 

  83. van der Aa, HA (1973) Studies in Phyllosticta. Stud Mycol 5: 1–110

    Google Scholar 

  84. Vánky, K (2004) New smut fungi (Ustilaginomycetes) from Mexico, and the genus Lundquistia. Fungal Divers 17: 159–190

    Google Scholar 

  85. van Ryckegem, G, Verbeken, A (2005) Fungal ecology and succession on Phragmites australis in a brackish tidal marsh. I. Leaf sheaths. Fungal Divers 19: 157–187

    Google Scholar 

  86. Vettraino, AM, Paolacci, A, Vannini, A (2005) Entophytism of Sclerotinia pseudotuberosa: PCR assay for specific detection in chestnut tissues. Mycol Res 109: 96–102

    Article  PubMed  CAS  Google Scholar 

  87. West, JS, Kharbanda, PD, Barbetti, MJ, Fitt, BDL (2001) Epidemiology and management of Leptosphaeria maculans (phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathol 50: 10–27

    Article  Google Scholar 

  88. Whalley, AJS (1996) The xylariaceaous way of life. Mycol Res 100: 897–922

    Article  Google Scholar 

  89. White, TJ, Bruns, TD, Lee, S, Taylor, JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, MA, Gelfand, DH, Sninsky, JS, White, TJ (Eds.) PCR Protocols: A Guide to Methods and Applications. Acardemic Press, New York, pp 315–322

    Google Scholar 

  90. Whitton, SR, McKenzie, EHC, Hyde, KD (2002) Microfungi on the Pandanaceae: Two new species of Camposporium, and a key to the genus. Fungal Divers 11: 177–187

    Google Scholar 

  91. Whitton, SR, McKenzie, EHC, Hyde, KD (2003) Microfungi on the Pandanaceae: Zygosporium, a review of the genus and two new species. Fungal Divers 12: 207–222

    Google Scholar 

  92. Wong, MKM, Hyde, KD (2001) Diversity of fungi on six grasses species of Gramineae and one species of Cyperaceae in Hong Kong. Mycol Res 105: 1485–1491

    Google Scholar 

  93. Yanna, Ho, WH, Hyde, KD (2002) Fungal succession on fronds of Phoenix hanceana in Hong Kong. Fungal Divers 10: 185–211

    Google Scholar 

  94. Yanna, Hyde, KD (2002) New saprobic fungi on palms fronds from north Queensland, Australia. Aust Syst Bot 15: 755–764

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Hong Kong Research Grants Council and the University of Hong Kong for providing funds (HKU 7322/04M; CRCG 10205773) to Dr. R. Jeewon and Dr K.D. Hyde to carry out the molecular work and manuscript preparation, and for providing support to I. Promputtha with a training studentship and D. Vijaykrishna with a studentship. Funds for this research were also provided by the Royal Golden Jubilee Ph.D. Program (4.B.CM/44/D.1) under the Thailand Research Fund. S. Lumyong thanks JSPS-NRCT (2003–2005) for support. Shenoy B.D., Helen Leung, and Heidi Kong are thanked for assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rajesh Jeewon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Promputtha, I., Lumyong, S., Dhanasekaran, V. et al. A Phylogenetic Evaluation of Whether Endophytes Become Saprotrophs at Host Senescence. Microb Ecol 53, 579–590 (2007). https://doi.org/10.1007/s00248-006-9117-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9117-x

Keywords

Navigation