Fungal Diversity

, Volume 54, Issue 1, pp 1–10 | Cite as

Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review

  • Cyd E. HamiltonEmail author
  • P. E. Gundel
  • M. Helander
  • K. Saikkonen


Reactive oxygen species are in all types of organisms from microbes to higher plants and animals. They are by-products of normal metabolism, such as photosynthesis and respiration, and are responsive to abiotic and biotic stress. Accumulating evidence suggests reactive oxygen species play a vital role in programmed cell death, stress responses, plant defense against pathogens and systemic stress signaling in conjunction with antioxidant production. Here, we propose that reactive oxygen species and antioxidants, as both universal and evolutionarily conserved, are likely to play important role(s) in symbiotic interactions. To support this hypothesis we review the root and foliar fungal endophyte literature specific to fungal-plant symbiotum production of reactive oxygen species and antioxidants in response to stress. These asymptomatic fungi can produce antioxidants in response to both biotic and abiotic stress when grown in culture as well as in planta. In addition, there is a growing but nascent literature reporting a significant impact of endophyte colonization on the antioxidant activity of colonized (E+) hosts when compared to uncolonized (E-) hosts, especially when exposed to stress. Here we summarize general patterns emerging from the growing literature specific to antioxidant activity of endophytes in colonized hosts and bring up possible future research questions and approaches. The consequences of changes in reactive oxygen species production and increased antioxidant activity in the symbiotum appear to be beneficial in many instances; but costs are also indicated. Unexplored questions are: 1) to what extent do antioxidants originating from the fungal endophyte mediate host metabolism, and thereby control host responses to endophyte colonization; (2) what role do fungal, plant, or symbiotum produced reactive oxygen species and antioxidants have in determining symbiotic outcome between extremes of pathogenicity and mutualism; and (3) what role if any, do the production of reactive oxygen species and their antioxidant counterparts play in the symbiotum’s ability to respond to changing selection pressures? If as the literature suggests, such endophyte imposed mediation can be utilized to foster increases in plant production in resource limited habitats then the utilization of fungal endophytes may prove useful in agronomic and conservation settings.


Endophyte Symbiosis Neotyphodium Epichloë Mutualism Dark septate endophytes Antagonism Stress Pathogen 



We thank Dr. Kirk Overmyer for helpful discussion about host physiology in response to stress; Drs. Jaakko Kangasjäarvi and Mikael Brosché as well as Springer Publishing for permission to modify their published figures (see Fig. 2); and two anonymous referees for helpful comments.


  1. Agarwal S (2007) Increased antioxidant activity in Cassia seedlings under UV-B radiation. Biol Plant 511:157–160CrossRefGoogle Scholar
  2. Ahlholm JU, Heland M, Lehtimäki, Wäli P, Saikkonen K (2000) Vertically transmitted fungal endophytes: Different responses of host-parasite systems to environmental conditions. Oikos 99:173–183Google Scholar
  3. Andrade-Linares DR, Grosch R, Restrepo S, Krumbein A, Franken P (2011) Effects of dark septate endophytes on tomato plant performance. Mycorrhiza 21:413–22PubMedCrossRefGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Rev Plant Physiol 55:373–99Google Scholar
  5. Asai T, Guillaume T, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–83PubMedCrossRefGoogle Scholar
  6. Bae H, Sicher RC, Moon SK, Kim S-H, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. Exp Bot 60:3279–2395CrossRefGoogle Scholar
  7. Baltruschat H, Fodor J, Harrach BD, Niemczk E, Barna B, Gullner G, Janeczko A, Kogel K-H, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510PubMedCrossRefGoogle Scholar
  8. Bartholdy BA, Berreck M, Haselwandter K (2001) Hydoxamate siderophores synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. BioMetals 14:33–42PubMedCrossRefGoogle Scholar
  9. Bonnet M, Camares O, Veisseire P (2000) Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp Bot 51:945–53PubMedCrossRefGoogle Scholar
  10. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51CrossRefGoogle Scholar
  11. Broshce M, Overmyer K, Wrzaczek M, Kangasjärvi J (2009) Stress signaling III: reactive oxygen species. In: Pareek A, Sopory S, Bohnert H, Govindjee (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer, Berlin, pp 91–102Google Scholar
  12. Calderón AA, Zapata JM, Romualdo M, Pedreño MA, Barceló AR (1993) Resveratrol production as a part of the hypersensitive-like response of grapevine cells to an elicitor from Trichoderma viride. New Phytol 124:455–463CrossRefGoogle Scholar
  13. Cázares E, Trappe JM, Jumpponen A (2005) Mycorrhiza-plant colonization patterns on a subalpine glacier forefront as a model system of primary succession. Mycorrhiza 15:405–16PubMedCrossRefGoogle Scholar
  14. Chacón MR, Rodríguez-Galán O, Benítez T, Sousa S, Rey M, Llobell A, Delgado-Jarana J (2007) Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int Microbiol 10:19–27PubMedGoogle Scholar
  15. Cheplick GP, Faeth SH (2009) Ecology and evolution of the grass-endophyte symbiosis. Oxford University Press, Oxford, UKCrossRefGoogle Scholar
  16. Clarke BB, White JF, Hurley RH, Torres MS, Sun S, Huff DR (2006) Endophyte-mediated suppression of dollar spot disease in fine fescues. Plant Dis 90:994–998CrossRefGoogle Scholar
  17. Clay K (1993) The ecology and evolution of endophytes. Agr Ecosyst Environ 44:39–64CrossRefGoogle Scholar
  18. De Gara L, Locato V, Dipierro S, de Pinto MC (2010) Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Respir Physiol Neurobiol 173:S13–9PubMedCrossRefGoogle Scholar
  19. Debbab A, Aly AH, Proksch P (2011) Bioactive secondary metabolites from endophytes and associated marine derived fungi. Fungal Divers 49:1–12CrossRefGoogle Scholar
  20. Eaton CJ, Jourdain I, Foster SJ, Hyams JS, Scott B (2008) Functional analysis of a fungal endophyte stress-activated MAP kinase. Curr Genet 53:163–164PubMedCrossRefGoogle Scholar
  21. Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenesis? Plant Sci 180:190–5PubMedCrossRefGoogle Scholar
  22. Foyer CH, Noctor G (2000) Tansley Review No. 112 Oxygen processing in photosynthesis: regulation and signaling. New Phytol 112:359–388CrossRefGoogle Scholar
  23. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  24. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18PubMedCrossRefGoogle Scholar
  25. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100PubMedCrossRefGoogle Scholar
  26. Gaber A, Yoshimura K, Yamamoto T, Yabuta Y, Takeda T, Miyasaka H, Nakano Y, Shigeoka S (2006) Glutathione peroxidase-like protein of Synechocystis PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis. Physiol Plantarum 128:251–262CrossRefGoogle Scholar
  27. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–101PubMedCrossRefGoogle Scholar
  28. Gessler NN, Aver’yanov AA, Belozerskaya AA (2007) Reactive oxygen species in regulation of fungal development. Biochemistry 72:1091–1109PubMedGoogle Scholar
  29. 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 47:19–27CrossRefGoogle Scholar
  30. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930CrossRefGoogle Scholar
  31. González V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42CrossRefGoogle Scholar
  32. Grünig CR, Linde CC, Sieber TN, Rogers SO (2003) Development of single-copy RFLP markers for population genetic studies of Phialocephala fortinii and closely related taxa. Mycol Res 107:1332–1341PubMedCrossRefGoogle Scholar
  33. Gundel PE, Maseda PH, Vila-Aiub MM, Ghersa CM, Benech-Arnold R (2006) Effects of Neotyphodium fungi on Lolium multiflorum seed germination in relation to water availability. Ann Bot 95:571–7CrossRefGoogle Scholar
  34. Gundel PE, Omacini M, Sadras VO, Ghersa CM (2010) The interplay between the effectiveness of the grass-endophyte mutualism and the genetic variability of the host plant in an agronomic context. Evol Appl 3:538–546CrossRefGoogle Scholar
  35. Gundel PE, Zabalgogeazcoa I, Vázquez de Aldana BR (2011) Interaction between plant genotype and the symbiosis with Epichloë fungal endophytes in seeds of red fescue (Festuca rubra). Crop For Sci 62:1010–1016Google Scholar
  36. Gundel PE, Garibaldi LA, Martínez-Ghersa MA, Ghersa CM (2012) Trade-off between seed number and weight: influence of a grass-endophyte symbiosis. Basic Appl Ecol 13:32–39CrossRefGoogle Scholar
  37. Hahn HM, McManus T, Warnstorff K, Monahan BJ, Young CA, Davies E, Tapper BA, Scott B (2008) Neotyphodium fungal endophytes confer physiological protection to perennial ryegrass (Lolium perenne L.) subjected to a water deficit. Environ Exp Bot 63:183–199CrossRefGoogle Scholar
  38. Hamilton CE, Bauerle, TL (2012) A new currency for mutualism: Neotyphodium antioxidants and host drought response. Fungal DiversGoogle Scholar
  39. Hamilton CE, Faeth SH, Dowling TE (2009) Distribution of hybrid fungal symbionts and environmental stress. Microbial Ecol 58:408–413CrossRefGoogle Scholar
  40. Hamilton CE, Dowling TE, Faeth SH (2010) Hybridization in endophyte symbionts alters host response to moisture and nutrient treatments. Microb Ecol 59:768–75PubMedCrossRefGoogle Scholar
  41. Harman GE (2000) Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis 84:377–393CrossRefGoogle Scholar
  42. Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194PubMedCrossRefGoogle Scholar
  43. Harman GE (2011) Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol 189:647–649PubMedCrossRefGoogle Scholar
  44. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species - opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56PubMedCrossRefGoogle Scholar
  45. Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2003) Effects of Neotyphodium endophytes on growth, reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass Forage Sci 58:407–415CrossRefGoogle Scholar
  46. Hoque A, Banu NA, Okuma E, Amako K, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. J Plant Phys 164:1457–68CrossRefGoogle Scholar
  47. Huang W-Y, Cai Y-Z, Xing J, Corke H, Sun M (2007) A Potential antioxidant resource: endophytic fungi from medicinal plants. Econ Bot 61:14–30CrossRefGoogle Scholar
  48. Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plantarum 138:405–13CrossRefGoogle Scholar
  49. Jennings DB, Ehrenshaft M, Pharr DM, Williamson JD (1998) Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense. PNAS 95:15129–33PubMedCrossRefGoogle Scholar
  50. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism—parasitism continuum. New Phytol 135:575–585CrossRefGoogle Scholar
  51. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PNAS 107:2093–2098PubMedCrossRefGoogle Scholar
  52. Jumpponen A (1999) Spatial distribution of discrete RAPD fungus, phenotypes of a root endophytic Phialocephala fortinii, at a primary successional site on a glacier forefront. New Phytol 141:333–344CrossRefGoogle Scholar
  53. Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211CrossRefGoogle Scholar
  54. Jumpponen A, Jones KL (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513PubMedCrossRefGoogle Scholar
  55. Jumpponen A, Trappe JM (1998) Dark-septate root endophytes: a review with special reference to facultative biotrophic symbiosis. New Phytol 140:295–310CrossRefGoogle Scholar
  56. Kawasaki L, Sánchez O, Shiozaki K, Aguirre J (2002) SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans. Mol Microbiol 45:1153–63PubMedCrossRefGoogle Scholar
  57. Kogel K-H, Voll LM, Schäfer P, Jansen C, Wu Y, Langen G, Imani J et al (2010) Transcriptome and metabolome profiling of field-grown transgenic barley lack induced differences but show cultivar-specific variances. PNAS 107:6198–203PubMedCrossRefGoogle Scholar
  58. Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Planta 155:780–790Google Scholar
  59. Lehtonen P, Helander M, Saikkonen K (2005) Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia 142:38–45PubMedCrossRefGoogle Scholar
  60. Logan DC (2006) The mitochondrial compartment. J Exp Bot 57:1225–1243PubMedCrossRefGoogle Scholar
  61. Lohar DP, Haridas S, Gantt JS, VandenBosch KA (2007) A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol 173:39–49PubMedCrossRefGoogle Scholar
  62. Lyons PC, Evans JJ, Bacon CW (1990) Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiol 92:726–32PubMedCrossRefGoogle Scholar
  63. Mandyam K, Jumpponen A (2012) Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie. Mycorrhiza 22:109–119PubMedCrossRefGoogle Scholar
  64. Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821PubMedCrossRefGoogle Scholar
  65. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant:Three-way symbiosis required for thermal tolerance. Science 316:513–515CrossRefGoogle Scholar
  66. Matsouri F, Björkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Biol Control 100:1213–1221Google Scholar
  67. Medzhitov R, Janeway CA (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91:295–298PubMedCrossRefGoogle Scholar
  68. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–10PubMedCrossRefGoogle Scholar
  69. Molinari HBC, Marur CJ, Daros E, de Campos MKF, de Carvalho JFRP, Filho JCB, Pereira LFP, Vieira LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): Osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol Plantarum 130:218–229CrossRefGoogle Scholar
  70. Morse LJ, Faeth SH, Day TA (2007) Neotyphodium interactions with a wild grass are driven mainly by endophyte haplotype. Funct Ecol 21:813–822CrossRefGoogle Scholar
  71. Mouhamadou B, Molitor C, Baptist F, Sage L, Clément J-C, Lavorel S, Monier A, Geremia RA (2011) Differences in fungal communities associated to Festuca paniculata roots in subalpine grasslands. Fungal Divers 47:55–63CrossRefGoogle Scholar
  72. Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integ Plant Biol 52:95–204CrossRefGoogle Scholar
  73. Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–22CrossRefGoogle Scholar
  74. Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342PubMedCrossRefGoogle Scholar
  75. Pang C-H, Wang B-S (2010) Ascorbate-glutathione pathway and stress tolerance in plants. In: Chan M-T, Umar S (eds) Naser A. Stress, The International Journal on the Biology of Stress, Springer, pp 91–113Google Scholar
  76. Phongpaichit S, Nikom J, Rungjindamai N, Sakayaroj J, Hutadilok-Towatana N, Rukachaisirikul V, Kirtikara K (2007) Biological activities of extracts from endophytic fungi isolated from Garcinia plants. FEMS Immunol Med Microbiol 51:517–25PubMedCrossRefGoogle Scholar
  77. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathology 49:291–315CrossRefGoogle Scholar
  78. Postma JWM, Olsson PA, Falkengren-Grerup U (2007) Root colonisation by arbuscular mycorrhizal, fine endophytic and dark septate fungi across a pH gradient in acid beech forests. Soil Biol Biochem 39:400–408CrossRefGoogle Scholar
  79. Purahong W, Hyde KD (2011) Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7CrossRefGoogle Scholar
  80. Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiol 146:1440–1453PubMedCrossRefGoogle Scholar
  81. Rasmussen S, Parsons A, Newman JA (2009) Metabolomics analysis of the Lolium perenne-Neotyphodium lolii symbiosis: more than just alkaloids? Phytochem Rev 8:535–550CrossRefGoogle Scholar
  82. Read DJ, Haselwandter K (1981) Observations on the mycorrhizal status of some alpine plant communities. New Phytol 88:341–352CrossRefGoogle Scholar
  83. Redman RS, Dunigan D, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: Who controls the outcome, host or invader ? New Phytol 151:705–716CrossRefGoogle Scholar
  84. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581–1581PubMedCrossRefGoogle Scholar
  85. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823PubMedCrossRefGoogle Scholar
  86. Rocha ACS, Garcia D, Uetanabaro APT, Carneiro RTO, Araujo IS, Mattos CRR, Goes-Neto A (2011) Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Divers 47:75–84CrossRefGoogle Scholar
  87. Rodriguez RJ, Redman R (2005) Balancing the generation and elimination of reactive oxygen species. PNAS 102:3175–3176PubMedCrossRefGoogle Scholar
  88. Rodriguez RJ, 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 59:1109–1114PubMedCrossRefGoogle Scholar
  89. Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitigation Adapt Strat Global Change 9:261–272CrossRefGoogle Scholar
  90. Rodriguez RJ, Henson J, van Volkenburgh E, Hoy M, Wright L, Beckwith F, Yong-Ok K, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefGoogle Scholar
  91. Rouhier N, Jacquot J-P (2008) Getting sick may help plants overcome abiotic stress. New Phytol 180:738–741PubMedCrossRefGoogle Scholar
  92. Rudgers JA, Afkhami ME, Rúa MA, Davitt AJ, Hammer S, Huguet VM (2009) A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology 90:1531–1539PubMedCrossRefGoogle Scholar
  93. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74CrossRefGoogle Scholar
  94. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal Endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343CrossRefGoogle Scholar
  95. Saikkonen K, Helander M, Faeth SH (2004) Fungal endophytes: hitch-hikers of the green world. In: Gillings M, Holmes A (eds) Plant Microbiology. Routledge, UK, pp 77–95Google Scholar
  96. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433PubMedCrossRefGoogle Scholar
  97. Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113CrossRefGoogle Scholar
  98. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340PubMedCrossRefGoogle Scholar
  99. Scholes JD, Lee PJ, Horton P, Lewis DH (1994) Invertase: understanding changes in the photosynthetic and carbohydrate metabolism of barley leaves infected with powdery mildew. New Phytol 126:213–222CrossRefGoogle Scholar
  100. Shao H-B, Chu L-Y, Lu Z-H, Kang C-M (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14CrossRefGoogle Scholar
  101. Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminum toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864PubMedCrossRefGoogle Scholar
  102. Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. MPMI 21:799–807PubMedCrossRefGoogle Scholar
  103. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227PubMedCrossRefGoogle Scholar
  104. Shittu HO, Castroverde DCM, Nazar RN, Robb J (2009) Plant-endophyte interplay protects tomato against a virulent Verticillium. Planta 229:415–426PubMedCrossRefGoogle Scholar
  105. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43PubMedCrossRefGoogle Scholar
  106. Simon-Sarkadi L, Kocsy G, Várhegyi Á, Galiba G, Ronde JA (2006) Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biol Plantarum 50:793–796CrossRefGoogle Scholar
  107. Smith DC (1979) From extracellular to intracellular: the establishment of a symbiosis. PNAS 204:115–130Google Scholar
  108. Smith IK, Thomas L, Vierheller TCA (1989) Properties and functions of glutathione reductase in plants. Physiol Plantarum 77:449–456CrossRefGoogle Scholar
  109. Srinivasan K, Jagadish LK, Shenbhagaraman R, Muthumary J (2010) Antioxidant activity of endophytic fungus Phyllosticta sp. isolated from Guazuma tomentosa. J Phytol Phytochem 2:37–41Google Scholar
  110. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol R 67:491–502CrossRefGoogle Scholar
  111. Sullivan TJ, Faeth SH (2008) Local adaptation in Festuca arizonica infected by hybrid and nonhybrid Neotyphodium endophytes. Microbial Ecol 55:697–704CrossRefGoogle Scholar
  112. Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017PubMedCrossRefGoogle Scholar
  113. Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29:1061–1076PubMedCrossRefGoogle Scholar
  114. Tanaka A, Christensen MJ, Takemoto D, Pyoyun P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066PubMedCrossRefGoogle Scholar
  115. Tanaka A, Takemoto D, Hyon G-S, Park P, Scott B (2008) NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass. Mol Microbiol 68:1165–1178PubMedCrossRefGoogle Scholar
  116. Tejesvi MV, Kajula M, Mattila S, Pirttilä AM (2011) Bioactivity and genetic diversity of endophytic fungi in Rhododendron tomentosum Harmaja. Fungal Divers 47:97–107CrossRefGoogle Scholar
  117. Torres MA (2010) ROS in biotic interactions. Physiol Plantarum 138:414–429CrossRefGoogle Scholar
  118. Torres MA, Jones JDJ, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378PubMedCrossRefGoogle Scholar
  119. Torres MA, White JF, Zhang X, Hinton DM, Bacon CW (2012) Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Funct Ecol in press Google Scholar
  120. Udayanga D, Liu XZ, McKenzie EHC, Chukeatorate E, Bahkali HA, Hyde KD (2011) The genus Phomopsis: biology, species concepts, future and names of important phytopathogens. Fungal Divers 50:189–225CrossRefGoogle Scholar
  121. Vesterlund SR, Helander M, Faeth SH, Hyvönen T, Saikkonen K (2011) Environmental conditions and host plant origin override endophyte effects on invertebrate communities. Fungal Divers 47:109–118CrossRefGoogle Scholar
  122. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS 102:13386–13391PubMedCrossRefGoogle Scholar
  123. White JF, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plantarum 138:440–446CrossRefGoogle Scholar
  124. Wikee S, Udayanga D, Crous PW, Chukeatirote E, McKenzie EHC, Bahkali AH, Dai DQ, Hyde KD (2011) Phyllosticta—an overview of current status of species recognition. Fungal Divers 51:43–61CrossRefGoogle Scholar
  125. Wilson D (1995) Endophyte—the evolution of a term, and clarification of its use and definition. Oikos 73:274–276CrossRefGoogle Scholar
  126. Yan Y, Han C, Liu Q, Lin B, Wang J (2008) Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiol Plant 30:433–440CrossRefGoogle Scholar
  127. Zhang YP, Nan ZB (2007) Growth and anti-oxidative systems changes in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci 193:377–386CrossRefGoogle Scholar
  128. Zhang YP, Nan ZB (2010) Germination and seedling anti-oxidative enzymes of endophyte-infected populations of Elymus dahuricus under osmotic stress. Seed Sci Technol 38:522–527Google Scholar

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© The Mushroom Research Foundation 2012

Authors and Affiliations

  • Cyd E. Hamilton
    • 1
    Email author
  • P. E. Gundel
    • 1
    • 2
  • M. Helander
    • 3
  • K. Saikkonen
    • 1
  1. 1.MTT Agrifood Research Finland, Plant Production ResearchJokioinenFinland
  2. 2.IFEVA - CONICET – Faculty of AgronomyBuenos Aires University (UBA)Buenos AiresArgentina
  3. 3.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland

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