Plant and Soil

, 346:363 | Cite as

Benefits of a symbiotic association with endophytic fungi are subject to water and nutrient availability in Achnatherum sibiricum

  • An Zhi Ren
  • Xia Li
  • Rong Han
  • Li Jia Yin
  • Mao Ying Wei
  • Yu Bao Gao
Regular Article


Symbiotic relationships with microbes may influence how plants respond to environmental change. Here, we investigated how fungal endophyte infection affected the growth of a native grass under altered water and nutrient availability. In a two-month field experiment, we compared the performance of endophyte-infected (EI) and endophyte-free (EF) Achnatherum sibiricum subjected to four treatments comprised of a factorial combination of two levels of water availability and two levels of fertilization. The greatest benefits of endophyte infection occurred in the well-watered fertilized treatment. With reduced water and/or nutrient availability, the benefits declined. EI plants subjected to drought and fertilization had higher root:shoot ratios and allocated more nitrogen to photosynthetic machinery and thus had a higher net photosynthetic rate than EF counterparts. In the well-watered unfertilized treatment, EF plants allocated more nutrients to photosynthetic machinery, while EI plants allocated more resources to defense. Thus EI plants were superior to EF plants in terms of nutrient conservation. In the drought unfertilized treatment, no significant difference occurred between EI and EF plants. Our results support the idea that the endophyte-grass interactions are dependent on available resources. However, we did not find a clear cost of endophyte infection. For A. sibiricum, fertilizer addition resulted in greater benefits of the symbiosis for plant growth, but this advantage decreased under drought.


Endophyte infection Achnatherum sibiricum Drought Nutrient Interaction 



This research was funded by the National Key Basic Research Special Foundation (No. 2007CB106802), the National Natural Science Foundation (30970460), the Doctoral Program Foundation of Institutions of Higher Education of China (20090031110026), and the Scientific Research Foundation for Returned Overseas Chinese Scholars, State Education Ministry (2009–2011).


  1. Ahlholm JU, Helander M, Lehtimaki S, Wali P, Saikkonen K (2002) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 99:173–183CrossRefGoogle Scholar
  2. Arachevaleta M, Bacon CW, Hoveland CS, Radcliffe E (1989) Effect of the tall fescue endophyte on plant response to environmental stress. Agron J 81:83–90CrossRefGoogle Scholar
  3. Belesky DP, Devine OJ, Pallas JE Jr, Stringer WE (1987) Photosynthetic activity of tall fescue as influenced by a fungal endophyte. Photosynthetica 21:82–87Google Scholar
  4. Bruehl GW, Kaiser WJ, Klenin RE (1994) An endophyte of Achnatherum inebrians, an intoxicating grass of northwest China. Mycologia 86:773–776CrossRefGoogle Scholar
  5. Buck GW, Elbersen HW, West CP, Sleper DA (1994) Endophyte enhances drought survival of Moroccan fescues. Arkansas Farm Res 43:6–7Google Scholar
  6. Cheplick GP (2004) Symbiotic fungi and clonal plant physiology. New Phytol 164:413–415CrossRefGoogle Scholar
  7. Cheplick GP (2007) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exp Bot 60:202–210CrossRefGoogle Scholar
  8. Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97CrossRefGoogle Scholar
  9. Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A et al (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304Google Scholar
  10. Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131:61–67CrossRefGoogle Scholar
  11. Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 98:25–36CrossRefGoogle Scholar
  12. Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett 7:304–313CrossRefGoogle Scholar
  13. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 11:191–210Google Scholar
  14. Feng YL, Fu GL, Zheng YL (2007) Specific leaf area relates to the differences in leaf construction cost, photosynthesis, nitrogen allocation, and use efficiencies between invasive and noninvasive alien congeners. Planta 228:383–390CrossRefGoogle Scholar
  15. Hahn H, McManus MT, 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
  16. Hakes AS, Cronin JT (2011) Environmental heterogeneity and spatiotemporal variability in plant defense traits. Oikos 120:452–462CrossRefGoogle Scholar
  17. Hesse U, Schoberlein W, Wittenmayer L, Forster 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
  18. Hesse U, Schoberlein W, Wittenmayer L, Forster K, Warnstorff K, Diepenbrock W, Merbach W (2005) Influence of water supply and endophyte infection on vegetative and reproductive growth of two Lolium perenne L. genotypes. Eur J Agron 22:45–54CrossRefGoogle Scholar
  19. Jin XM, Han GD (2010) Effects of grazing intensity on species diversity and structure of meadow steppe community. Pratacultural Sci (in Chinese) 27(4):7–10Google Scholar
  20. Kannadan S, Rudgers JA (2008) Endophyte symbiosis benefits a rare grass under low water availability. Funct Ecol 22:706–713CrossRefGoogle Scholar
  21. Kurokawa H, Peltzer DA, Wardle DA (2010) Plant traits, leaf palatability and litter decomposability for co-occurring woody species differing in invasion status and nitrogen fixation ability. Funct Ecol 24:513–523CrossRefGoogle Scholar
  22. Laisk A (1977) Kinetics photosynthesis and photorespiration in C3 plants. Nauka, MoscowGoogle Scholar
  23. Latch GCM, Christensen MJ, Samuels GJ (1984) Five endophytes of Lolium and Festuca in New Zealand. Mycotaxon 20:535–550Google Scholar
  24. Lewis GC (2004) Effects of biotic and abiotic stress on the growth of three genotypes of Lolium perenne with and without infection by the fungal endophyte Neotyphodium lolii. Ann Appl Biol 144:53–63CrossRefGoogle Scholar
  25. Li X, Han R, Ren AZ, Gao YB (2010) Using high-temperature treatment to construct endophyte-free Achnatherum sibiricum. Microbiol China 37:1395–1400Google Scholar
  26. Lin FP, Chen ZH, Chen ZP, Zhang DM (1999) Physiological and biochemical responses of the seedlings of four legume tree species to high CO2 concentration. Chin J Plant Ecol 23:220–22Google Scholar
  27. Loustau D, Beahim M, Gaudillère JP, Dreyer E (1999) Photosynthetic responses to phosphorous nutrition in two-year-old maritime pine seedlings. Tree Physiol 19:707–715PubMedGoogle Scholar
  28. Malinowski D, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  29. Malinowski DP, Alloush GA, Belesky DP (1998) Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil 205:1–12CrossRefGoogle Scholar
  30. Marks S, Clay K (2007) Low resource availability differentially affects the growth of host grasses infected by fungal endophytes. Int J Plant Sci 168:1269–1277CrossRefGoogle Scholar
  31. Marks S, Clay K, Cheplick GP (1991) Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne. J Appl Ecol 28:194–204CrossRefGoogle Scholar
  32. McCormick MK, Gross KL, Smith RA (2001) Danthonia spicata (Poaceae) and Atkinsonella hypoxylon (Balansiae): environmental dependence of a symbiosis. Am J Bot 88:903–909PubMedCrossRefGoogle Scholar
  33. Morse LJ, Day TA, Faeth SH (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environ Exp Bot 48:257–268CrossRefGoogle Scholar
  34. Morse LJ, Faeth SH, Day TA (2007) Neotyphodium interactions with a wild grass are driven mainly by endophyte haplotype. FunctEcol 21:813–822Google Scholar
  35. Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456PubMedCrossRefGoogle Scholar
  36. Niinemets Ü (2001) Climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs at the global scale. Ecology 82:453–469CrossRefGoogle Scholar
  37. Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866CrossRefGoogle Scholar
  38. Petroski RJ, Powell RG, Clay K (1992) Alkaloids of Stipa robusta (sleepygrass) infected with an Acremonium endophyte. Nat Toxins 1:84–88PubMedCrossRefGoogle Scholar
  39. Ravel C, Balfourier F, Guillaumin JJ (1999) Enhancement of yield and persistence of perennial ryegrass inoculated with one endophyte isolate in France. Agronomie 19:635–644CrossRefGoogle Scholar
  40. Read JC, Camp BJ (1986) The effect of fungal endophyte Acremonium coenophialum in tall fescue on animal performance, toxicity, and stand maintenance. Agron J 78:848–850CrossRefGoogle Scholar
  41. Ren AZ, Gao YB, Wang W, Wang JL, Zhao NX (2009) Influence of nitrogen fertilizer and endophyte infection on ecophysiological parameters and mineral element content of perennial ryegrass. J Integr Plant Biol 51:75–83PubMedCrossRefGoogle Scholar
  42. Rudgers JA, Swafford AL (2009) Benefits of a fungal endophyte in Elymus virginicus decline under drought stress. Basic Appl Ecol 10:43–51CrossRefGoogle Scholar
  43. Saona NM, Albrectsen BR, Ericson L, Bazely DR (2010) Environmental stresses mediate endophyte–grass interactions in a boreal archipelago. J Ecol 98:470–479CrossRefGoogle Scholar
  44. Spiering MJ, Greer DH, Schmid J (2006) Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann Bot 98:379–387PubMedCrossRefGoogle Scholar
  45. Wei YK, Gao YB, Xu H, Su D, Zhang X, Wang YH, Lin F, Chen L, Nie LY, Ren AZ (2006) Occurrence of endophytes in grasses native to northern China. Grass Forage Sci 61:422–429CrossRefGoogle Scholar
  46. West CP, Izekor E, Turner KE, Elmi AA (1993) Endophyte effects on growth and persistence of tall fescue along a water-supply gradient. Agron J 85:264–270CrossRefGoogle Scholar
  47. Wu ZL, Lu SL (1995) On geographical distribution of Achnatherum beauv. (Gramineae). Acta Phytotaxon Sin 34:152–161Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • An Zhi Ren
    • 1
  • Xia Li
    • 1
  • Rong Han
    • 1
  • Li Jia Yin
    • 1
  • Mao Ying Wei
    • 1
  • Yu Bao Gao
    • 1
  1. 1.College of Life SciencesNankai UniversityTianjinPeople’s Republic of China

Personalised recommendations