Journal of Chemical Ecology

, 34:1511 | Cite as

Effects of Methyl Jasmonate and an Endophytic Fungus on Plant Resistance to Insect Herbivores

  • Lacy Simons
  • Thomas L. Bultman
  • T. J. Sullivan


Tall fescue (Lolium arundinaceum) forms a mutualistic relationship with the fungal endophyte Neotyphodium coenophialum. The endophyte provides constitutive resistance to herbivores through its production of alkaloid compounds. Moreover, herbivore attack induces elevated synthesis of loline alkaloids, that is, the fungus also provides wound-inducible resistance for its host. Jasmonic acid and its conjugates are key signaling compounds in many plant species and play a role systemically in the upregulation of defensive compounds within plants following attack by herbivores. The purpose of our study was to determine if and how the plant and fungus respond to methyl jasmonate (MJ) exposure and if these responses interact in antagonistic or synergistic ways. Plants were exposed to MJ via gaseous diffusion within a controlled environment chamber. Response to MJ was assessed with an herbivore bioassay, gas chromatography–mass spectrometry to quantify alkaloids, and real-time reverse transcriptase-polymerase chain reaction to quantify mRNA from a loline alkaloid biosynthesis gene. We found that MJ hindered endophyte-infected tall fescue’s resistance against aphids by downregulating transcription of the LolC gene. The opposite pattern was observed for endophyte-free tall fescue; its exposure to MJ resulted in a significant increase in resistance to aphids, apparently through stimulating defense compounds produced by the plant. These results indicate that, when tall fescue lacks fungal infection, MJ induces the plant to produce its own defensive compounds. In contrast, while endophyte-infected plants are defended from herbivores by fungally produced lolines, this defense is compromised by MJ.


Alkaloid Endophyte Herbivory Jasmonic acid Lolium Tall fescue 



Several undergraduate students helped in counting aphids: T. Boman, A. Dreyer, D. Fraker, R. Johnson, N. Marra, B. McMahon, and J. Molenhouse. The Departments of Biology and Chemistry provided facilities. Financial support for this work was provided by NSF-URC award (0629174) to the City Colleges of Chicago and NSF-CRUI (DBI-0330840) award to TLB.


  1. Barnard, C., and Frankel, O. H. 1964. Grass, grazing animals, and man in historic perspective, pp. 1–12, in C. Barnard (ed.). Grasses and GrasslandsMacMillan, New York.Google Scholar
  2. Breen, J. 1994. Acremonium endophyte interactions with enhanced plant resistance to insects. Annu. Rev. Entomol. 39:401–423.CrossRefGoogle Scholar
  3. Bultman, T. L., Bell, G., and Martin, W. D. 2004. A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685.CrossRefGoogle Scholar
  4. Bush, L. P., Cornelius, P. L., Buckner, R. C., Varney, D. R., Chapman, R. A., Burriss, P. B. II, Kennedy, C. W., Jones, T. A., and Saunders, M. J. 1982. Association of N-acetyl loline and N-formyl loline with Epichloe typhina in tall fescue. Crop Science. 22:941–943.Google Scholar
  5. Bush, L. P., Fannin, F. F., Siegal, M. R., Dahlman, D. L., and Burton, H. R. 1993. Chemistry, occurrence and biological effects of saturated pyrrolizidine alkaloids associated with endophyte–grass interactions. Agric. Ecosyst. Environ. 44:81–102.CrossRefGoogle Scholar
  6. Bush, L. P., Wilkinson, H. H., and Schardl, C. L. 1997. Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol. 114:1–7.PubMedGoogle Scholar
  7. Cheplick, G. P., and Clay, K. 1988. Acquired chemical defences in grasses: the role of fungal endophytes. Oikos 52:309–318.CrossRefGoogle Scholar
  8. Clay, K. 1988. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology. 69:10–16.CrossRefGoogle Scholar
  9. Clay, K. 1990. Fungal endophytes of grasses. Annu. Rev. Ecol. Syst. 21:275–297.CrossRefGoogle Scholar
  10. Clay, K. 1991. Fungal endophytes, grasses, and herbivores., pp. 199–226, in P. Barbosa, V. A. Krischik, and C. G. Jones (eds.). Microbial Mediation of Plant–Herbivore InteractionsWiley, New York.Google Scholar
  11. Clement, S. L., Kaiser, W. J., and Eichenseer, H. 1994. Acremonium endophytes in germplasms of major grasses and their utilization for insect resistance, pp. 185–199, in C. W. Bacon, and J.F. White Jr. (eds.). Biotechnology of endophytic fungi of grassesCRC, Boca Raton.Google Scholar
  12. Conover, W. J., and Iman, R. L. 1981. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Statist. 35:124–129.CrossRefGoogle Scholar
  13. Creelman, R. A., and Mullet, J. E. 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:355–381.PubMedCrossRefGoogle Scholar
  14. de Bruxelles, G. L., and Roberts, M. R. 2001. Signals regulating multiple responses to wounding and herbivores. Critical Rev. Plant Sci. 20:487–521.CrossRefGoogle Scholar
  15. Eichenseer, H., Dahlman, D. L., and Bush, L. P. 1991. Influence of endophyte infection, plant age and harvest interval on Rhopalosiphum padi survival and its relation to quantity of N-formyl and N-acetyl loline in tall fescue. Entomol. Exp. Appl. 60:29–38.CrossRefGoogle Scholar
  16. Faeth, S. H., and Bultman, T. L. 2002. Endophytic fungi and interactions among host plants, herbivores, and natural enemies, pp. 89–123, in T. Tscharntke, and B.A. Hawkins (eds.). Multitrophic Level InteractionsCambridge University Press, Cambridge.Google Scholar
  17. Farmer, E. E., and Ryan, C. A. 1990. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. PNAS USA 87:7713–7716.PubMedCrossRefGoogle Scholar
  18. Farmer, E. E., and Ryan, C. A. 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134.PubMedCrossRefGoogle Scholar
  19. Gols, R., Roosjen, M., Dijkman, H., and Dicke, M. 2003. Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. J. Chem. Ecol. 29:2651–2666.PubMedCrossRefGoogle Scholar
  20. Gunlach, H., Muller, M. J., Kutchan, T. M., and Zenk, M. H. 1992. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc. Nat. Acad. Sci. USA 89:2389–2393.CrossRefGoogle Scholar
  21. Gutierrez, C., Castanera, P., and Torres, V. 1988. Wound-induced changes in DIMBOA (2,4 dihydroxy-7-methoxy-2H-1, 4 benzoxazin-3(4H)-one) concentration in maize plants caused by Sesamia nonagriodes (Lepidoptera: Noctuidae). Annals Appl. Biol. 113:447–454.CrossRefGoogle Scholar
  22. Hall, S. S., and Horton, R. F. 1994. Methyl jasmonate and bean leaf abscission. Plant Growth Reg. 14:187–192.CrossRefGoogle Scholar
  23. Karban, R., and Myers, J. H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. System. 20:331–348.CrossRefGoogle Scholar
  24. Keilholz, U., Willhauck, M., Rimoldi, D., Brasseur, F., Dummer, W., Rass, K., De Vries, T., Blaheta, J., Voit, C., Lethé, B., and Burchill, S. 1998. Reliability of reverse transcription-polymerase chain reaction (RT-PCR)-based assays for the detection of circulating tumor cells: a quality-assurance initiative of the EORTC Melanoma Cooperative Group. Eur. J. Cancer 34:750–753.PubMedCrossRefGoogle Scholar
  25. Klun, J. A., Tipton, C. L., and Brindley, T. A. 1967. 2,4-Dihydroxy-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA), an active agent in the resistance of maize to the European corn borer. J. Econom. Entomol. 60:1529–1533.Google Scholar
  26. Latch, G. C. M. 1993. Physiological interactions of endophytic fungi and their hosts: biotic stress tolerance imparted to grasses by endophytes. Agri. Ecosys. Environ. 44:143–156.CrossRefGoogle Scholar
  27. Leather, S. R., Walters, K. F. A., and Dixon, A. F. G. 1989. Factors determining the pest status of the bird cherry-oat aphid Rhopalosiphum padi (L.) (Homoptera: Aphididae), in Europe: a study and review. Bull. Entomol. Res. 79:345–360.CrossRefGoogle Scholar
  28. Lehtonen, P., Helander, M., and Saikkonen, K. 2005. Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia 142:38–45.PubMedCrossRefGoogle Scholar
  29. Lou, Y., Hua, X., Turlings, T., Cheng, J., Chen, X., and Ye, G. 2006. Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. J. Chem. Ecol. 32:2375–2387.PubMedCrossRefGoogle Scholar
  30. Matsui, K., Wilkinson, J., Hiatt, B., Knauf, V., and Kajiwara, T. 1999. Molecular cloning and expression of Arabidopsis fatty acid hydroperoxide lyase. Plant Cell Physiol. 40:477–481.PubMedGoogle Scholar
  31. McConn, M., Creelman, R. A., Bell, E., Mullet, J. E., and Browse, J. 1997. Jasmonate is essential for insect defense in Arabidopsis. Plant Biol. 94:5473–5477.Google Scholar
  32. Mei, C., Qi, M., Sheng, G., and Yang, Y. 2006. Inducible overexpression of a rice allene oxide synthetase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol. Plant Microbe Interact. 19:1127–1137.PubMedCrossRefGoogle Scholar
  33. Nott, H. M., and Latch, G. C. M. 1993. A simple method of killing endophyte in ryegrass seed, pp. 14–15, in D.E. Hume, G.C.M. Latch, and H.A. Easton (eds.). Proceedings of the 2nd International Symposium on Acremonium/Grass Interactions.AgResearch, Palmerston North.Google Scholar
  34. Reinbothe, S., Mollenhauer, B., and Reinbothe, C. 1994. Jips and rips—the regulation of plant gene-expression by jasmonates in response to environmental cues and pathogens. Plant Cell 6:1197–1209.PubMedCrossRefGoogle Scholar
  35. Russell, W. A., Guthrie, W. D., Klun, J. A., and Grindeland, R. 1975. Selection for resistance in maize to first-brood European corn borer by using leaf-feeding damage of the insect and chemical analysis for DIMBOA in the plant. J. Econ. Entomol. 68:31–34.Google Scholar
  36. Saikkonen, K., Faeth, S. H., Helander, M., and Sullivan, T. J. 1998. Fungal endophytes: a continuum of interactions with host plants. Annu. Rev. Ecol. Syst. 29:319–343.CrossRefGoogle Scholar
  37. Schardl, C. L., and Clay, K. 1997. Evolution of mutualistic endophytes from plant pathogens, pp. 221–238, in G. Carrol, and I.P. Tudzynski (eds.). The Mycota V: Plant Relationships, Part B Springer, Berlin.Google Scholar
  38. Schardl, C. L., Grossman, R. B., Nagabhyru, P., Faulkner, J. R., and Mallik, U. P. 2007. Loline alkaloids: currencies of mutualism. Phytochemistry 68:980–996.PubMedCrossRefGoogle Scholar
  39. Siegel, M. R., Latch, G. C. M., Bush, L. P., Fannin, F. F., and Rowan, D. D. 1990. Fungal endophyte-infected grasses—alkaloid accumulation and aphid response. J. Chem. Ecol. 16:3301–3315.CrossRefGoogle Scholar
  40. Spiering, M. J., Moon, C. D., Wilkinson, H. H., and Schardl, C. L. 2005. Gene clusters for insecticidal loline alkaloids in the grass endophytic fungus Neotyphodium uncinatum. Genetics 169:1403–1414.PubMedCrossRefGoogle Scholar
  41. Stebbins, G. L. 1981. Coevolution of grasses and herbivores. Annal. Missouri Bot. Gard. 68:75–86.CrossRefGoogle Scholar
  42. Sullivan, T. J., Rodstom, J., Vandop, J., Librizzi, J., Grahm, C., Schardl, C. L., and Bultman, T. L. 2007. Symbiont-mediated changes in Lolium arundinaceum inducible defenses: evidence from changes in gene expression and leaf composition. New Phytol. 176:673–679.PubMedCrossRefGoogle Scholar
  43. SYSTAT 2004. The System for Statistics. SYSTAT, Evanston.Google Scholar
  44. Thaler, J. A. 1999. Induced resistance in agricultural crops: effects of jasmonic acid on herbivory and yield in tomato plants. Environ. Entomol. 28:30–37.Google Scholar
  45. Wasternack, C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annal. Botany 100:681–697.CrossRefGoogle Scholar
  46. Wilkinson, H. H., Siegel, M. R., Blankenship, J. D., Mallory, A. C., Bush, L. P., and Schardl, C. L. 2000. Contribution of fungal loline alkaloids to protection from aphids in grass–endophyte mutualism. Am. Phytopathol. Soc. 13:1027–1033.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Lacy Simons
    • 1
    • 2
  • Thomas L. Bultman
    • 1
  • T. J. Sullivan
    • 3
  1. 1.Department of BiologyHope CollegeHollandUSA
  2. 2.Truman CollegeChicagoUSA
  3. 3.Hope CollegeHollandUSA

Personalised recommendations