Skip to main content
Log in

Chemical Ecology Mediated by Fungal Endophytes in Grasses

  • Review Article
  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Defensive mutualism is widely accepted as providing the best framework for understanding how seed-transmitted, alkaloid producing fungal endophytes of grasses are maintained in many host populations. Here, we first briefly review current knowledge of bioactive alkaloids produced by systemic grass-endophytes. New findings suggest that chemotypic diversity of the endophyte-grass symbiotum is far more complex, involving multifaceted signaling and chemical cross-talk between endophyte and host cells (e.g., reactive oxygen species and antioxidants) or between plants, herbivores, and their natural enemies (e.g., volatile organic compounds, and salicylic acid and jasmonic acid pathways). Accumulating evidence also suggests that the tight relationship between the systemic endophyte and the host grass can lead to the loss of grass traits when the lost functions, such as plant defense to herbivores, are compensated for by an interactive endophytic fungal partner. Furthermore, chemotypic diversity of a symbiotum appears to depend on the endophyte and the host plant life histories, as well as on fungal and plant genotypes, abiotic and biotic environmental conditions, and their interactions. Thus, joint approaches of (bio)chemists, molecular biologists, plant physiologists, evolutionary biologists, and ecologists are urgently needed to fully understand the endophyte-grass symbiosis, its coevolutionary history, and ecological importance. We propose that endophyte-grass symbiosis provides an excellent model to study microbially mediated multirophic interactions from molecular mechanisms to ecology.

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.

Fig. 1

Similar content being viewed by others

References

  • Agee CS, Hill NS (1994) Ergovaline variability in Acremonium -infected tall fescue due to environment and plant genotype. Crop Sci 34:221–226

    Article  Google Scholar 

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432

    Article  Google Scholar 

  • Agrawal AA, Fishbein M (2008) Phylogenetic escalation and decline of plant defense strategies. Proc Natl Acad Sci USA 105:10057–10060

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Rev Plant Physiol 55:373–399

    CAS  Google Scholar 

  • Arechavaleta M, Bacon CW, Plattner RD, Hoveland CS, Radcliffe DE (1992) Accumulation of ergopeptide alkaloids in symbiotic tall fescue grown under deficits of soil water and nitrogen fertilizer. Appl Environ Microb 58:857–861

    CAS  Google Scholar 

  • Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microb 34:576–581

    CAS  Google Scholar 

  • Ball OJ-P, Prestidge RA, Sprosen JM (1995) Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Appl Environ Microb 61:1527–1533

    CAS  Google Scholar 

  • Ballare CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16:249–257

    Article  PubMed  CAS  Google Scholar 

  • Belesky DP, Stuedemann JA, Plattner RD, Wilkinson SR (1988) Ergopeptine alkaloids in grazed tall fescue. Agron J 80:209–212

    Article  CAS  Google Scholar 

  • Boning RA, Bultman TL (1996) A Test for constitutive and induced resistance by tall fescue (Festuca arundinacea) to an insect herbivore: Impact of the fungal endophyte, Acremonium coenophialum. Am Midl Nat 136:328–335

    Article  Google Scholar 

  • Bultman TL, Bell G, Martin WD (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685

    Article  Google Scholar 

  • Cheplick GP, Faeth S (2009) Ecology and evolution of the grassendophyte symbiosis. Oxford University Press, New York

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297

    Article  Google Scholar 

  • Clay K (2009) Defensive mutualism and grass endophytes: still valid after all these years? pp. 9–20 in Torres M and White Jr. JF (eds.). Defensive mutualism in symbiotic association. Taylor and Francis Publications

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744

    Article  PubMed  CAS  Google Scholar 

  • Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:s99–s127

    Article  PubMed  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant anti-herbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • di Menna ME, Waller JE (1986) Visual assessment of seasonal changes in amount of mycelium of Acremonium loliae in leaf sheaths of perennial ryegrass. New Zeal J Agr Res 29:111–116

    Article  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175

    Article  PubMed  CAS  Google Scholar 

  • Easton HS, Latch GCM, Tapper BA, Ball OJ-P (2002) Ryegrass host genetic control of concentrations of endophyte-derived alkaloids. Crop Sci 42:51–57

    Article  PubMed  CAS  Google Scholar 

  • Eaton CJ, Cox MP, Ambrose B, Becker M, Hesse U, Schardl CL, Scott B (2010) Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiol 153:1780–1794

    Article  PubMed  CAS  Google Scholar 

  • Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180:190–195

    Article  PubMed  CAS  Google Scholar 

  • Eich E, Pertz H (1999) Antimicrobial and antitumor effects of ergot alkaloids and their derivates. In: Kren V, Cvak L (eds) Ergot: the genus Claviceps. Harwood Academic Publishers, Amsterdam, pp 441–449

    Google Scholar 

  • Ellers J, Kiers ET, Currie CR, McDonald BR, Visser B (2012) Ecological interactions drive evolutionary loss of traits. Ecol Lett 15:1071–1082

    Article  PubMed  Google Scholar 

  • Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann NY Acad Sci 503:295–306

    Article  PubMed  CAS  Google Scholar 

  • Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 99:200

    Article  Google Scholar 

  • Faeth SH, Fagan WF (2002) Fungal endophytes: common host plant symbionts but uncommon mutualists. Integ Comp Biol 42:360–368

    Article  Google Scholar 

  • Faeth SH, Shochat E (2010) Inherited microbial symbionts increase herbivore abundances and alter arthropod diversity on a native grass. Ecology 91:1329–1343

    Article  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Gundel PE, Hamilton CE, Seal CE, Helander M, Martinez-Ghersa MA, Ghersa CM, Vazquez de Aldana BR, Zabalgogeazcoa I, Saikkonen K (2012) Antioxidants in Festuca rubra L. seeds affected by the fungal symbiont Epichloë festucae. Symbiosis 58:73–80

    Article  Google Scholar 

  • Hamilton C, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10

    Article  Google Scholar 

  • Hovermale JT, Craig AM (2001) Correlation of ergovaline and lolitrem B levels in endophyte-infected perennial ryegrass (Lolium perenne). J Vet Diagn Invest 13:323–327

    Article  PubMed  CAS  Google Scholar 

  • Huitu O, Helander M, Lehtonen P, Saikkonen K (2008) Consumption of grassendophytes alters the ultraviolet spectrum of vole urine. Oecologia 156:333–340

    Article  PubMed  Google Scholar 

  • Jani AJ, Faeth SH (2010) Asexual endophytes and associated alkaloids alter arthropod community structure and increase herbivore abundances on a native grass. Ecol Lett 13:106–117

    Article  PubMed  Google Scholar 

  • Jensen JG, Popay AJ (2004) Perennial ryegrass infected with AR37 endophyte reduces survival of porina larvae. New Zeal Plant Prot 57:323–328

    Google Scholar 

  • Justus M, Write L, Hartmann T (1997) Levels and tissue distribution of loline alkaloids in endophyte-infected Festuca pratensis. Phytochemistry 44:51–57

    Article  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Latch GCM (1994) Influence of Acremonium endophytes on perennial grass improvement. New Zeal J Agr Res 37:311–318

    Article  Google Scholar 

  • Lemons A, Clay K, Rudgers JA (2005) Connecting plant–microbial interactions above and belowground:a fungal endophyte affects decomposition. Oecologia 145:595–604

    Article  PubMed  Google Scholar 

  • Leuchtmann A, Schmidt D, Bush LP (2000) Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophytes. J Chem Ecol 26:1025–1036

    Article  CAS  Google Scholar 

  • Liu Q, Parson AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol 25:910–920

    Article  Google Scholar 

  • Lyons PC, Plattner RD, Bacon CW (1986) Occurrence of peptide and clavine ergot alkaloids in tall fescue grass. Science 232:487–489

    Article  PubMed  CAS  Google Scholar 

  • Malinowski DP, Belesky DP, Hill NS, Baligar VC, Fedders JM (1998) Influence of phosphorus on the growth and ergot alkaloid content of Neotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb.). Plant Soil 198:53–61

    Article  CAS  Google Scholar 

  • Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133:727–733

    Article  Google Scholar 

  • Massey FP, Hartley SE (2006) Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates. Proc R Soc Lond B 273:2299–2304

    Article  CAS  Google Scholar 

  • McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310

    Article  Google Scholar 

  • McNaughton SJ (1984) Grazing lawns: animals in herds, plant form, and coevolution. Am Nat 124:863–886

    Article  Google Scholar 

  • Miranda MI, Omacini M, Chaneton EJ (2011) Environmental context of endophyte symbioses: interacting effects of water stress and insect herbivory. Int J Plant Sci 172:499–508

    Article  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 13:1455–1467

    Article  PubMed  CAS  Google Scholar 

  • Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactiveoxygen species during plant-microorganism early interactions. J Integ Plant Biol 52:95–204

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81

    Article  PubMed  CAS  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Otero P (2004) Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos 104:581–590

    Article  Google Scholar 

  • Panaccione DG, Beaulieu WT, Cook D (2013) Bioactive alkaloids in vertically transmitted fungal endophytes. Funct Ecol. doi:10.1111/1365-2435.12076

    Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  PubMed  CAS  Google Scholar 

  • Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Funct Ecol. doi:10.1111/1365-2435.12050

    Google Scholar 

  • Popay AJ, Gerard PJ (2007) Cultivar and endophyte effects on a root aphid, Aploneura lentisci, in perennial ryegrass. New Zeal Plant Prot 60:223–227

    Google Scholar 

  • Prasad V, Strömberg CAE, Alimohammadian H, Sahni A (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science 310:1177–1180

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol 173:787–797

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen S, Liu Q, Parsons AJ, Xue H, Sinclair B, Newman JA (2012) Grass– endophyte interactions: a note on the role of monosaccharide transport in the Neotyphodium loliiLolium perenne symbiosis. New Phytol 196:7–12

    Article  PubMed  CAS  Google Scholar 

  • Richardson MD, Hoveland CS, Bacon CW (1993) Photosynthesis and stomatal conductance of symbiotic and nonsymbiotic tall fescue. Crop Sci 33:145–149

    Article  Google Scholar 

  • Rodriguez RJ, Redman R (2005) Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci USA 102:3175–3176

    Article  PubMed  CAS  Google Scholar 

  • 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 59:1109–1114

    Article  PubMed  CAS  Google Scholar 

  • Romeo JT, Saunders JA, Barbosa P (eds) (1996) Phytochemical diversity and redundancy in ecological interactions. Plenum Press, New York

    Google Scholar 

  • Rudgers JA, Fischer S, Clay K (2010) Managing plant symbioses: fungal endophyte genotype alters plant community composition. J Appl Ecol 47:468–477

    Article  Google Scholar 

  • Saari S, Helander M, Wallius E, Saikkonen K (2010a) Fungal endophytes reduce regrowth and affect competitiveness of meadow ryegrass in early succession. Grass Forage Sci 65:287–295

    Google Scholar 

  • Saari S, Sundell J, Huitu O, Helander M, Ketoja E, Ylönen H, Saikkonen K (2010b) Fungal-mediated multitrophic interactions - do grass endophytes in diet protect voles from predators? PLoS One 5:e9845. doi:10.1371/journal.pone.0009845

    Article  PubMed  Google Scholar 

  • Saikkonen K (2000) Kentucky-31, far from home. Science 17:1887a

    Article  Google Scholar 

  • Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280

    Article  PubMed  CAS  Google Scholar 

  • Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433

    Article  PubMed  CAS  Google Scholar 

  • Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113

    Article  Google Scholar 

  • Saikkonen K, Ruokolainen K, Huitu O, Gundel PE, Piltti T, Hamilton CE, Helander M (2013) Fungal endophytes help prevent weed invasions. Agr Ecosyst Environ 165:1–5

    Article  Google Scholar 

  • Schardl CL, Young CA, Faulkner JR, Florea S, Pan J (2012) Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol 5:331–344

    Article  Google Scholar 

  • Siegel MR, Bush LP (1996) Defensive chemicals in grass–fungal endophyte associations. Rec Adv Phytochem 30:81–118

    CAS  Google Scholar 

  • Siegel MR, Latch GCM, Bush LP, Fannin FF, Rowan DD, Tapper BA, Bacon CW, Johnson MC (1990) Fungal endophyte infected grasses: alkaloid accumulation and aphid response. J Chem Ecol 16:3301–3314

    Article  CAS  Google Scholar 

  • Simons L, Bultman TL, Sullivan TJ (2008) Effects of methyl jasmonate and an endophytic fungus on plant resistance to insect herbivores. J Chem Ecol 34:1511–1517

    Article  PubMed  CAS  Google Scholar 

  • Spiering MJ, Lane GA, Christensen MJ, Schmid J (2005) Distribution of the fungal endophyte Neotyphodium lolii is not a major determinant of the distribution of fungal alkaloids in Lolium perenne plants. Phytochemistry 66:195–202

    Article  PubMed  CAS  Google Scholar 

  • Stewart AV (2005) The commercial use of endophyte in turf ryegrass in New Zealand. Int Turfgrass Soc Res J 10:641–644

    Google Scholar 

  • Sullivan TJ, Rodstrom J, Vandop J, Librizzi J, Graham C, Schardl CL, Bultman TL (2007) Symbiont-mediated changes in Lolium arundinaceum inducible defenses: Evidence from changes in gene expression and leaf composition expression and leaf composition. New Phytol 176:673–679

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050

    Article  PubMed  CAS  Google Scholar 

  • 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 18:1052–1066

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Takemoto D, Hyon G-S, Park P, Scott B (2008) NoxA activation by the small GTPaseRacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass. Mol Microbiol 68:1165–1178

    Article  PubMed  CAS  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  PubMed  CAS  Google Scholar 

  • Thompson JN (2005) The geographic mosaic theory of coevolution. University of Chicago Press

  • Van Der Meijden E, Wijn M, Verkaar HJ (1988) Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363

    Article  Google Scholar 

  • Vázquez de Aldana BR, Zabalgogeazcoa I, García Ciudad A, García Criado B (2003) Ergovaline occurrence in grasses infected by fungal endophytes of semi-arid pastures in Spain. J Sci Food Agric 83:347–353

    Article  Google Scholar 

  • Vázquez de Aldana BR, Zabalgogeazcoa I, De Casas Rubio R, García Ciudad A, García Criado B (2009) Relationships between the genetic distance of Epichloë festucae isolates and the ergovaline and peramine contents of their Festuca rubra hosts. Ann Appl Biol 156:51–61

    Article  Google Scholar 

  • Vesterlund S-R, Helander M, Faeth SH, Hyvönen T, Saikkonen K (2011) Environmental conditions and host plant origin override endophyte effects on invertebrate communities. Fungal Divers 47:109–118

    Article  Google Scholar 

  • Vicari M, Bazely DR (1993) Do grasses fight back? The case for antiherbivore defences. Trends Ecol Evol 8:137–141

    Article  PubMed  CAS  Google Scholar 

  • Wäli PR, Helander M, Nissinen O, Saikkonen K (2006) Susceptibility of endophyte-infected grasses to winter pathogens (snow moulds). Can J Bot 84:1043–1051

    Article  Google Scholar 

  • White JF, Torres MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446

    Article  PubMed  CAS  Google Scholar 

  • Xiao Y, Wang Q, Erb M, Turlings Tc, Ge L, Hu L, Li J, Han X, Zhang T, Lu J, Zhang G, Lou Y (2012) Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett 15:1130–1139

    Article  PubMed  CAS  Google Scholar 

  • Zhang D-X, Nagabhyru P, Schardl CL (2009) Regulation of a chemical defense against herbivory produced by symbiotic fungi in grass plants. Plant Physiol 150:1072–1082

    Article  PubMed  CAS  Google Scholar 

  • Zhang D-X, Nagabhyru P, Blankenship JD, Schardl CL (2010) Are loline alkaloid levels regulated in grass endophytes by gene expression or substrate availability? Plant Signal Behav 5:1–4

    Article  Google Scholar 

Download references

Acknowledgments

We thank Stan Faeth for valuable comments on the manuscript. This study was funded by the Academy of Finland (Project no. 137909).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kari Saikkonen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saikkonen, K., Gundel, P.E. & Helander, M. Chemical Ecology Mediated by Fungal Endophytes in Grasses. J Chem Ecol 39, 962–968 (2013). https://doi.org/10.1007/s10886-013-0310-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-013-0310-3

Keywords

Navigation