, Volume 22, Issue 2, pp 109–119 | Cite as

Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie

  • Keerthi Mandyam
  • Chad Fox
  • Ari JumpponenEmail author
Original Paper


Native tallgrass prairies support distinct dark septate endophyte (DSE) communities exemplified by Periconia macrospinosa and Microdochium sp. that were recently identified as common root symbionts in this system. Since these DSE fungi were repeatedly isolated from grasses and forbs, we aimed to test their abilities to colonize different hosts. One Microdochium and three Periconia strains were screened for colonization and growth responses using five native grasses and six forbs in an in vitro system. Previously published data for an additional grass (Andropogon gerardii) were included and reanalyzed. Presence of indicative inter- and intracellular structures (melanized hyphae, microsclerotia, and chlamydospores) demonstrated that all plant species were colonized by the DSE isolates albeit to varying degrees. Microscopic observations suggested that, compared to forbs, grasses were colonized to a greater degree in vitro. Host biomass responses varied among the host species. In broad comparisons, more grass species than forbs tended to respond positively to colonization, whereas more forb species tended to be non-responsive. Based on the suspected differences in the levels of colonization, we predicted that tallgrass prairie grasses would support greater DSE colonization than forbs in the field. A survey of field-collected roots from 15 native species supported this hypothesis. Our study supports the “broad host range” of DSE fungi, although the differences in the rates of colonization in the laboratory and in the field suggest a greater compatibility between grasses and DSE fungi. Furthermore, host responses to DSE range from mutualism to parasitism, suggesting a genotype-level interplay between the fungi and their hosts that determines the outcome of this symbiosis.


Dark septate endophytes (DSE) Mycorrhizal dependency Mutualism–parasitism continuum 



This work was supported in part by NSF DEB-0344838 (to AJ). Konza Prairie Biological Research Station maintained the field sites and was supported by National Science Foundation Long Term Ecological Research (LTER) program. Chad Fox completed the microscopic analyses as a part of Konza Prairie LTER “Research Experiences for Undergraduates” program. Richard Wynia at the United States Department of Agriculture Natural Resources Conservation service provided some of the native seeds for the described studies. Authors thank Justin Trowbridge for assistance in acquiring the field-collected materials.


  1. Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13. doi: 10.1139/B04-171 CrossRefGoogle Scholar
  2. Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470. doi: 10.1007/s11104-009-0125-8 CrossRefGoogle Scholar
  3. Barrow JR, Aaltonen RE (2001) Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11:199–205CrossRefGoogle Scholar
  4. Fernando AA, Currah RS (1996) A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture. Can J Bot 74:1071–1078CrossRefGoogle Scholar
  5. 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 102:1012–1026. doi: 10.3852/09-264 PubMedCrossRefGoogle Scholar
  6. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. doi: 10.1111/j.1461-0248.2009.01430.x PubMedCrossRefGoogle Scholar
  7. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  8. Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211CrossRefGoogle Scholar
  9. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310CrossRefGoogle Scholar
  10. Kageyama SA, Mandyam KG, Jumpponen A (2008) Diversity, function and potential applications of the root-associated endophytes. In: Varma A (ed) Mycorrhiza—state of the art, genetics and molecular biology, eco-function, biotechnology, ecophysiology, structure and systematics. Springer, Berlin, pp 29–59Google Scholar
  11. Karst J, Marczak L, Jones MD, Turkington R (2008) The mutualism–parasitism continuum in ectomycorrhizas: a quantitative assessment using meta-analysis. Ecology 89:1032–1042PubMedCrossRefGoogle Scholar
  12. Karst J, Jones MD, Turkington R (2009) Ectomycorrhizal colonization and intraspecific variation in growth responses of lodgepole pine. Plant Ecol 200:161–165. doi: 10.1007/s11258-008-9443-9 CrossRefGoogle Scholar
  13. Khidir HH, 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
  14. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  15. Kogel K, Franken P, Hueckelhoven R (2006) Endophyte or parasite—what decides? Curr Opin Plant Biol 9:358–363. doi: 10.1016/j.pbi.2006.05.001 PubMedCrossRefGoogle Scholar
  16. Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189CrossRefGoogle Scholar
  17. Mandyam K, Jumpponen A (2008) Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza 18:145–155. doi: 10.1007/s00572-008-0165-6 PubMedCrossRefGoogle Scholar
  18. Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821. doi: 10.3852/09-212 PubMedCrossRefGoogle Scholar
  19. Mcgonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501CrossRefGoogle Scholar
  20. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364. doi: 10.1111/j.1469-8137.2004.01169.x CrossRefGoogle Scholar
  21. Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol. doi: 10.1111/j.1469-8137.2010.03611.x PubMedGoogle Scholar
  22. O'Dell TE, Massicotte HB, Trappe JM (1993) Root colonization of Lupinus latifolius Agardh and Pinus contorta Dougl by Phialocephala fortinii Wang and Wilcox. New Phytol 124:93–100CrossRefGoogle Scholar
  23. Philips JM, Hayman DA (1970) Improved procedures for clearing and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  24. Piculell BJ, Hoeksema JD, Thompson JN (2008) Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. BMC Biol 6:23. doi: 10.1186/1741-7007-6-23 PubMedCrossRefGoogle Scholar
  25. 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
  26. Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Appl Environ Microbiol 74:2805–2813. doi: 10.1128/AEM.02769-07 PubMedCrossRefGoogle Scholar
  27. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716CrossRefGoogle Scholar
  28. Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114. doi: 10.1093/jxb/erm342 PubMedCrossRefGoogle Scholar
  29. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416. doi: 10.1038/ismej.2007.106 PubMedCrossRefGoogle Scholar
  30. Schadt CW, Mullen RB, Schmidt SK (2001) Isolation and phylogenetic identification of a dark-septate fungus associated with the alpine plant Ranunculus adoneus. New Phytol 150:747–755CrossRefGoogle Scholar
  31. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686. doi: 10.1017/S095375620500273X PubMedCrossRefGoogle Scholar
  32. Schulz B, Rommert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte–host interaction: a balanced antagonism? Mycol Res 103:1275–1283CrossRefGoogle Scholar
  33. Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus–perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066. doi: 10.1105/tpc.105.039263 PubMedCrossRefGoogle Scholar
  34. Towne EG (2002) Vascular plants of Konza Prairie Biological Station: an annotated checklist of species in a Kansas tallgrass prairie. Sida 20:269–294Google Scholar
  35. Weishampel PA, Bedford BL (2006) Wetland dicots and monocots differ in colonization by arbuscular mycorrhizal fungi and dark septate endophytes. Mycorrhiza 16:495–502. doi: 10.1007/s00572-006-0064-7 PubMedCrossRefGoogle Scholar
  36. Wilcox HE, Wang CJK (1987) Ectomycorrhizal and ectendomycorrhizal associations of Phialophora finlandia with Pinus resinosa, Picea rubens, and Betula alleghaniensis. Can J For Res 17:976–990CrossRefGoogle Scholar
  37. Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Division of BiologyKansas State UniversityManhattanUSA

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