Evidence for Volatile Memory in Plants: Boosting Defence Priming through the Recurrent Application of Plant Volatiles

  • Received : 2018.03.08
  • Accepted : 2018.05.03
  • Published : 2018.08.31


Plant defence responses to various biotic stresses via systemic acquired resistance (SAR) are induced by avirulent pathogens and chemical compounds, including certain plant hormones in volatile form, such as methyl salicylate and methyl jasmonate. SAR refers to the observation that, when a local part of a plant is exposed to elicitors, the entire plant exhibits a resistance response. In the natural environment, plants are continuously exposed to avirulent pathogens that induce SAR and volatile emissions affecting neighbouring plants as well as the plant itself. However, the underlying mechanism has not been intensively studied. In this study, we evaluated whether plants "memorise" the previous activation of plant immunity when exposed repeatedly to plant defensive volatiles such as methyl salicylate and methyl jasmonate. We hypothesised that stronger SAR responses would occur in plants treated with repeated applications of the volatile plant defence compound MeSA than in those exposed to a single or no treatment. Nicotiana benthamiana seedlings subjected to repeated applications of MeSA exhibited greater protection against Pseudomonas syringae pv. tabaci and Pectobacterium carotovorum subsp. carotovorum than the control. The increase in SAR capacity in response to repeated MeSA treatment was confirmed by analysing the defence priming of the expression of N. benthamiana Pathogenesis-Related 1a (NbPR1a) and NbPR2 by quantitative reverse-transcription PCR compared with the control. We propose the concept of plant memory of plant defence volatiles and suggest that SAR is strengthened by the repeated perception of volatile compounds in plants.


Supported by : Rural Development Administration (RDA), Ministry of Science and ICT


  1. Bruce, T.J., Matthes, M.C., Napier, J.A., and Pickett, J.A. (2007). Stressful "memories" of plants: evidence and possible mechanisms. Plant Sci. 173, 603-608.
  2. Cameron, R.K., Paiva, N.L., Lamb, C.J., and Dixon, R.A. (1999). Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR). response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55, 121-130.
  3. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S., and Dong, X. (1997). The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57-63.
  4. Chanda, B., Xia, Y., Mandal, M.K., Yu, K., Sekine, K.T., Gao, Q.-m., Selote, D., Hu, Y., Stromberg, A., and Navarre, D. (2011). Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat. Genet. 43, 421-427.
  5. Chaturvedi, R., Venables, B., Petros, R.A., Nalam, V., Li, M., Wang, X., Takemoto, L.J., and Shah, J. (2012). An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 71, 161-172.
  6. Chen, M.S. (2008). Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15, 101-114.
  7. Choi, H.K., Song, G.C., Yi, H.-S., and Ryu, C.-M. (2014). Field evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. J. Chem. Ecol. 40, 882-892.
  8. Conrath, U., Beckers, G.J., Langenbach, C.J., and Jaskiewicz, M.R. (2015). Priming for enhanced defense. Annu. Rev. Phytopathol. 53, 97-119.
  9. Crisp, P.A., Ganguly, D., Eichten, S.R., Borevitz, J.O., and Pogson, B.J. (2016). Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2, e1501340.
  10. Fu, Z.Q., and Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839-863.
  11. Gao, Q.-M., Zhu, S., Kachroo, P., and Kachroo, A. (2015). Signal regulators of systemic acquired resistance. Front. Plant Sci. 6, 228.
  12. Giron-Calva, P.S., Molina-Torres, J., and Heil, M. (2012). Volatile dose and exposure time impact perception in neighboring plants. J. Chem. Ecol. 38, 226-228.
  13. Hammond-Kosack, K.E., and Jones, J. (1996). Resistance genedependent plant defense responses. Plant Cell 8, 1773.
  14. Heil, M., and Baldwin, I.T. (2002). Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61-67.
  15. Heil, M., and Bueno, J.C.S. (2007). Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 104, 5467-5472.
  16. Heil, M., and Adame-Alvarez, R.M. (2010). Short signalling distances make plant communication a soliloquy. Biology Lett. 6, 843-845.
  17. Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J., and Greenberg, J.T. (2009). Priming in systemic plant immunity. Science 324, 89-91.
  18. Karban, R., Shiojiri, K., Huntzinger, M., and McCall, A.C. (2006). Damage-induced resistance in sagebrush: volatiles are key to intraand interplant communication. Ecology 87, 922-930.[922:DRISVA]2.0.CO;2
  19. Kim, M., Ahn, J.-W., Jin, U.-H., Choi, D., Paek, K.-H., and Pai, H.-S. (2003). Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J. Biol. Chem. 278, 19406-19415.
  20. Kim, H., Kojima, M., Choi, D., Park, S., Matsui, M., Sakakibara, H., and Hwang, I. (2016). Overexpression of INCREASED CAMBIAL ACTIVITY, a putative methyltransferase, increases cambial activity and plant growth. J. Inteqr. Plant Biol. 58, 874-889.
  21. Kost, C., and Heil, M. (2006). Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J. Ecol. 94, 619-628.
  22. Kunkel, B.N., and Brooks, D.M. (2002). Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325-331.
  23. Ling, Q., Huang, W., and Jarvis, P. (2011). Use of a SPAD-502 meter to measure leaf chlorophyll concentration in Arabidopsis thaliana. Photosynth. Res. 107, 209-214.
  24. Ludwig-Muller, J., Julke, S., Geiss, K., Richter, F., Mithofer, A., Sola, I., Rusak, G., Keenan, S., and Bulman, S. (2015). A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid. Mol. Plant Pathol. 16, 349-364.
  25. Lyon, G. (2007). Agents that can elicit induced resistance. Induced resistance for plant defence. A sustainable approach to crop protection. Blackwell Publishing Ltd, Oxford, 9-29.
  26. Mandal, M.K., Chandra-Shekara, A., Jeong, R.-D., Yu, K., Zhu, S., Chanda, B., Navarre, D., Kachroo, A., and Kachroo, P. (2012). Oleic acid-dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide-mediated defense signaling in Arabidopsis. Plant Cell 24, 1654-1674.
  27. Martinez-Medina, A., Flors, V., Heil, M., Mauch-Mani, B., Pieterse, C.M., Pozo, M.J., Ton, J., van Dam, N.M., and Conrath, U. (2016). Recognizing plant defense priming. Trends Plant Sci. 21, 818-822.
  28. Mur, L.A., Kenton, P., Atzorn, R., Miersch, O., and Wasternack, C. (2006). The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140, 249-262.
  29. Navarova, H., Bernsdorff, F., Doring, A.-C., and Zeier, J. (2012). Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24, 5123-5141.
  30. Park, S.-W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D.F. (2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-116.
  31. Shah, J., and Zeier, J. (2013). Long-distance communication and signal amplification in systemic acquired resistance. Front. Plant Sci. 4, 30.
  32. Shah, J., Chaturvedi, R., Chowdhury, Z., Venables, B., and Petros, R.A. (2014). Signaling by small metabolites in systemic acquired resistance. Plant J. 79, 645-658.
  33. Shulaev, V., Silverman, P., and Raskin, I. (1997). Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 386, 718-721.
  34. Song, G.C., and Ryu, C.-M. (2013). Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int. J. Mol. Cell 14, 9803-9819.
  35. Song, G.C., Ryu, S.Y., Kim, Y.S., Lee, J.Y., Choi, J.S., and Ryu, C.-M. (2013). Elicitation of induced resistance against Pectobacterium carotovorum and Pseudomonas syringae by specific individual compounds derived from native Korean plant species. Molecules 18, 12877-12895.
  36. Van Bel, A.J., and Gaupels, F. (2004). Pathogen-induced resistance and alarm signals in the phloem. Mol. Plant Pathol. 5, 495-504.
  37. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., Uknes, S., Kessmann, H., and Ryals, J. (1994). Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6, 959-965
  38. Wildermuth, M.C., Dewdney, J., Wu, G., and Ausubel, F.M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562-565.
  39. Yi, H.-S., Heil, M., Adame-Álvarez, R.M., Ballhorn, D.J., and Ryu, C.-M. (2009). Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151, 2152-2161.