Journal of Chemical Ecology

, Volume 40, Issue 7, pp 816–825 | Cite as

Symptomless Endophytic Fungi Suppress Endogenous Levels of Salicylic Acid and Interact With the Jasmonate-Dependent Indirect Defense Traits of Their Host, Lima Bean (Phaseolus lunatus)

  • Ariana L. Navarro-Meléndez
  • Martin Heil


Symptomless ‘type II’ fungal endophytes colonize their plant host horizontally and exert diverse effects on its resistance phenotype. Here, we used wild Lima bean (Phaseolus lunatus) plants that were experimentally colonized with one of three strains of natural endophytes (Bartalinia pondoensis, Fusarium sp., or Cochliobolus lunatus) to investigate the effects of fungal colonization on the endogenous levels of salicylic acid (SA) and jasmonic acid (JA) and on two JA-dependent indirect defense traits. Colonization with Fusarium sp. enhanced JA levels in intact leaves, whereas B. pondoensis suppressed the induction of endogenous JA in mechanically damaged leaves. Endogenous SA levels in intact leaves were significantly decreased by all strains and B. pondoensis and Fusarium sp. decreased SA levels after mechanical damage. Colonization with Fusarium sp. or C. lunatus enhanced the number of detectable volatile organic compounds (VOCs) emitted from intact leaves, and all three strains enhanced the relative amount of several VOCs emitted from intact leaves as well as the number of detectable VOCs emitted from slightly damaged leaves. All three strains completely suppressed the induced secretion of extrafloral nectar (EFN) after the exogenous application of JA. Symptomless endophytes interact in complex and strain-specific ways with the endogenous levels of SA and JA and with the defense traits that are controlled by these hormones. These interactions can occur both upstream and downstream of the defense hormones.


Endophyte Extrafloral nectar Jasmonic acid Plant-fungus interaction Salicylic acid Volatile organic compounds 



We thank Priscila Chaverri and James Blande for sharing unpublished data, Catalina Estrada and an anonymous referee for comments on an earlier version of this manuscript, Wilhelm Boland for providing us with DMNT and TMTT and Jorge Molina for standard compounds and help with the chromatography. CONACyT of México is gratefully acknowledged for financial support to AN-M (300752) and to MH (project grants: 109621 and 130656).

Supplementary material

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  1. Ahlholm J, Helander M, Elamo P, Saloniemi I, Neuvonen S, Hanhimaki S, Saikkonen K (2002) Micro-fungi and invertebrate herbivores on birch trees: fungal mediated plant-herbivore interactions or responses to host quality? Ecol Lett 5:648–655CrossRefGoogle Scholar
  2. Albrectsen BR, Bjorken L, Varad A, Hagner A, Wedin M, Karlsson J, Jansson S (2010) Endophytic fungi in European aspen (Populus tremula) leaves-diversity, detection, and a suggested correlation with herbivory resistance. Fungal Divers 41:17–28CrossRefGoogle Scholar
  3. Ángeles-López YI, Martínez-Gallardo NA, Ramírez-Romero R, López MG, Sánchez-Hernández C, Délano-Frier JP (2013) Cross-kingdom effects of plant-plant signaling via volatile organic compounds emitted by tomato (Solanum lycopersicum) plants infested by the greenhouse whitefly (Trialeurodes vaporariorum). J Chem Ecol 38:1376–1386CrossRefGoogle Scholar
  4. Arnold AE (2007) Understanding the diversity of foliar fungal endophytes: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66CrossRefGoogle Scholar
  5. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: Are tropical leaves biodiversity hotspots? Ecology 88:541–549PubMedCrossRefGoogle Scholar
  6. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274CrossRefGoogle Scholar
  7. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654PubMedCentralPubMedCrossRefGoogle Scholar
  8. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297CrossRefGoogle Scholar
  9. Delaye L, García-Guzmán G, Heil M (2013) Endophytes versus biotrophic and necrotrophic pathogens - are fungal lifestyles evolutionarily stable traits? Fungal Divers 60:125–135CrossRefGoogle Scholar
  10. Estrada C, Wcislo WT, Van Bael SA (2013) Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytol 198:241–251PubMedCrossRefGoogle Scholar
  11. Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 98:25–36CrossRefGoogle Scholar
  12. Fröhlich J, Hyde KD, Petrini O (2000) Endophytic fungi associated with palms. Mycol Res 104:1202–1212CrossRefGoogle Scholar
  13. Gange AC, Eschen R, Wearn JA, Thawer A, Sutton BC (2012) Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant. Oecologia 168:1023–1031PubMedCrossRefGoogle Scholar
  14. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity of basidiomycetes:application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118PubMedCrossRefGoogle Scholar
  15. Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254CrossRefGoogle Scholar
  16. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 323–342Google Scholar
  17. Heil M (2004) Induction of two indirect defences benefits Lima bean (Phaseolus lunatus, Fabaceae) in nature. J Ecol 92:527–536CrossRefGoogle Scholar
  18. Heil M (2014) Relevance versus reproducibility-solving a common dilemma in chemical ecology. J Chem Ecol 40:315–316PubMedCrossRefGoogle Scholar
  19. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefGoogle Scholar
  20. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci U S A 104:5467–5472PubMedCentralPubMedCrossRefGoogle Scholar
  21. Jaber LR, Vidal S (2009) Interactions between an endophytic fungus, aphids and extrafloral nectaries: do endophytes induce extrafloral-mediated defences in Vicia faba? Funct Ecol 23:707–714CrossRefGoogle Scholar
  22. Jaber LR, Vidal S (2010) Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecol Entomol 35:25–36CrossRefGoogle Scholar
  23. Jallow MA, Dugassa-Gobena D, Vidal S (2008) Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthopod Plant Interact 2:53–62CrossRefGoogle Scholar
  24. Kost C, Heil M (2005) Increased availability of extrafloral nectar reduces herbivory in Lima beans (Phaseolus lunatus, Fabaceae). Basic Appl Ecol 6:237–248CrossRefGoogle Scholar
  25. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628CrossRefGoogle Scholar
  26. Kost C, Heil M (2008) The defensive role of volatile emission and extrafloral nectar secretion for Lima bean in nature. J Chem Ecol 34:2–13PubMedCentralCrossRefGoogle Scholar
  27. Kusumoto D, Matsumura E (2012) Effects of salicylic acid, 1-aminocyclopropan-1-carboxylic acid and methyl jasmonate on the frequencies of endophytic fungi in Quercus serrata leaves. For Pathol 42:393–396CrossRefGoogle Scholar
  28. Li T, Blande JD, Gundel PE, Helander M, Saikkonen K (2014) Epichloë endophytes alter inducible indirect defences in host grasses. PLOS ONE 9:e101331Google Scholar
  29. Malamy J, Henning J, Klessig DF (1992) Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4:359–366PubMedCentralPubMedCrossRefGoogle Scholar
  30. Mejía LC, Rojas EI, Maynard Z, Van Bael SA, Arnold AE, Hebbar P, Samuels GJ, Robbins N, Herre EA (2008) Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biol Control 46:4–14CrossRefGoogle Scholar
  31. Mucciarelli M, Camusso W, Maffei M, Panicco P, Bicchi C (2007) Volatile terpenoids of endophyte-free and infected peppermint (Mentha piperita L.): chemical partitioning of a symbiosis. Microb Ecol 54:685–696PubMedCrossRefGoogle Scholar
  32. Mueller MJ, Brodschelm W (1994) Quantification of jasmonic acid by capillary gas chromatography-negative chemical ionization-mass spectrometry. Anal Biochem 218:425–435PubMedCrossRefGoogle Scholar
  33. Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Biocontrol 55:113–128CrossRefGoogle Scholar
  34. Pańka D, Piesik D, Jeske M, Baturo-Cieśniewska A (2013) Production of phenolics and the emission of volatile organic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a response to infection by Fusarium poae. J Plant Physiol 170:1010–1019PubMedCrossRefGoogle Scholar
  35. Partida-Martinez LPP, Heil M (2011) The microbe-free plant: fact or artefact? Front Plant Sci 2:100Google Scholar
  36. Pluskota WE, Qu N, Maitrejean M, Boland W, Baldwin IT (2007) Jasmonates and its mimics differentially elicit systemic defence responses in Nicotiana attenuata. J Exp Bot 58:4071–4082PubMedCrossRefGoogle Scholar
  37. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398PubMedCrossRefGoogle Scholar
  38. Pozo MJ, Van Loon LC, Pieterse CMJ (2005) Jasmonates - signals in plant-microbe interactions. J Plant Growth Regul 23:211–222Google Scholar
  39. Ramírez-Chávez E, López-Bucio J, Herrera-Estrella L, Molina-Torres J (2004) Alkamides isolated from plants promote growth and alter root development in Arabidopsis. Plant Physiol 134:1058–1068PubMedCentralPubMedCrossRefGoogle Scholar
  40. Ren C-G, Dai C-C (2012) Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. BMC Plant Biol 12:128Google Scholar
  41. Saikkonen K, Wali P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280PubMedCrossRefGoogle Scholar
  42. Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968PubMedCrossRefGoogle Scholar
  43. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89CrossRefGoogle Scholar
  44. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270PubMedCrossRefGoogle Scholar
  45. Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of Ascomycetes and Basidiomycetes in environmental samples. PLoS One 7:e40863PubMedCentralPubMedCrossRefGoogle Scholar
  46. Van Bael SA, Estrada C, Rehner SA, Santos JF, Wcislo WT (2012) Leaf endophyte load influences fungal garden development in leaf-cutting ants. BMC Ecol 12:23PubMedCentralPubMedCrossRefGoogle Scholar
  47. Van Bael SA, Valencia MC, Rojas EI, Gomez N, Windsor DM, Herre EA (2009) Effects of foliar endophytic fungi on the preference and performance of the leaf beetle Chelymorpha alternans in Panama. Biotropica 41:221–225CrossRefGoogle Scholar
  48. Yuan ZL, Zhang CL, Lin FC (2010) Role of diverse non-systemic fungal endophytes in plant performance and response to stress: progress and approaches. J Plant Growth Regul 29:116–126CrossRefGoogle Scholar
  49. Yue Q, Wang CL, Gianfagna TJ, Meyer WA (2001) Volatile compounds of endophyte-free and infected tall fescue (Festuca arundinacea Schreb.). Phytochemistry 58:935–941Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Departamento de Ingeniería Genética, CINVESTAV-IrapuatoIrapuatoMexico

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