Journal of Chemical Ecology

, Volume 45, Issue 2, pp 136–145 | Cite as

Methyl Jasmonate Changes the Composition and Distribution Rather than the Concentration of Defence Compounds: a Study on Pyrrolizidine Alkaloids

  • Xianqin WeiEmail author
  • Klaas Vrieling
  • Patrick P. J. Mulder
  • Peter G. L. Klinkhamer


In this study we investigated the effect of methyl jasmonate (MeJA) application on pyrrolizidine alkaloid (PA) concentration and composition of two closely related Jacobaea species. In addition, we examined whether MeJA application affected herbivory of the polyphagous leaf feeding herbivore Spodoptera exigua. A range of concentrations of MeJA was added to the medium of Jacobaea vulgaris and J. aquatica tissue culture plants grown under axenic conditions. PA concentrations were measured in roots and shoots using LC-MS/MS. In neither species MeJA application did affect the total PA concentration at the whole plant level. In J. vulgaris the total PA concentration decreased in roots but increased in shoots. In J. aquatica a similar non-significant trend was observed. In both Jacobaea species MeJA application induced a strong shift from senecionine- to erucifoline-like PAs, while the jacobine- and otosenine-like PAs remained largely unaffected. The results show that MeJA application does not necessarily elicits de novo synthesis, but rather leads to PA conversion combined with reallocation of certain PAs from roots to shoots. S. exigua preferred feeding on control leaves of J. aquatica over MeJA treated leaves, while for J. vulgaris both the control and MeJA treated leaves were hardly eaten. This suggests that the MeJA-induced increase of erucifoline-like PAs can play a role in resistance of J. aquatica to S. exigua. In J. vulgaris resistance to S. exigua may already be high due to the presence of jacobine-like PAs or other resistance factors.


Conversion Erucifoline Feeding damage Herbivory Induced defense Jacobaea plants Reallocation Seneciphylline 



We thank Karin van der Veen-van Wijk for technical help with the tissue cultures. We thank Dr. Erica Wilson and Blair Bergere for their efforts on English polishing. We also thank Dr. Nicole van Dam and an anonymous reviewer for their valuable comments. Xianqin Wei was supported financially by the China Scholarship Council.

Supplementary material

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ESM 1 (PDF 551 kb)
10886_2018_1020_MOESM2_ESM.docx (29 kb)
ESM 2 (DOCX 29 kb)


  1. Berenbaum MR, Nitao JK, Zangerl AR (1991) Adaptive significance of furanocoumarin diversity in Pastinaca sativa (Apiaceae). J Chem Ecol 17:207–215CrossRefGoogle Scholar
  2. Bruinsma M, van Dam NM, van Loon JJA, Dicke M (2007) Jasmonic acid-induced changes in Brassica oleracea affect oviposition preference of two specialist herbivores. J Chem Ecol 33:655–668. CrossRefGoogle Scholar
  3. Chen H, Jones AD, Howe GA (2006) Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Lett 580:2540–2546CrossRefGoogle Scholar
  4. Cheng D, Kirk H, Mulder PPJ, Vrieling K, Klinkhamer PGL (2011a) Pyrrolizidine alkaloid variation in shoots and roots of segregating hybrids between Jacobaea vulgaris and Jacobaea aquatica. New Phytol 192:1010–1023CrossRefGoogle Scholar
  5. Cheng D, Kirk H, Vrieling K, Mulder PPJ, Klinkhamer PGL (2011b) The relationship between structurally different pyrrolizidine alkaloids and western flower thrips resistance in F2 hybrids of Jacobaea vulgaris and Jacobaea aquatica. J Chem Ecol 37:1071–1080CrossRefGoogle Scholar
  6. Cheng D, van der Meijden E, Mulder PPJ, Vrieling K, Klinkhamer PGL (2013) Pyrrolizidine alkaloid composition influences cinnabar moth oviposition preferences in Jacobaea hybrids. J Chem Ecol 39:430–437CrossRefGoogle Scholar
  7. Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378CrossRefGoogle Scholar
  8. Gershenzon J, McConkey ME, Croteau RB (2000) Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol 122:205–214CrossRefGoogle Scholar
  9. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227CrossRefGoogle Scholar
  10. Gundlach H, Müller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89:2389–2393CrossRefGoogle Scholar
  11. Hartmann T (1999) Chemical ecology of pyrrolizidine alkaloids. Planta 207:483–495CrossRefGoogle Scholar
  12. Hartmann T, Dierich B (1998) Chemical diversity and variation of pyrrolizidine alkaloids of the senecionine type: biological need or coincidence? Planta 206:443–451CrossRefGoogle Scholar
  13. Hartmann T, Toppel G (1987) Senecionine N-oxide, the primary product of pyrrolizidine alkaloid biosynthesis in root cultures of Senecio vulgaris. Phytochemistry 26:1639–1643CrossRefGoogle Scholar
  14. Hartmann T, Ehmke A, Eilert U, Borstel K, Theuring C (1989) Sites of synthesis, translocation and accumulation of pyrrolizidine alkaloid N-oxides in Senecio vulgaris L. Planta 177:98–107CrossRefGoogle Scholar
  15. Henery ML, Wallis IR, Stone C, Foley WJ (2008) Methyl jasmonate does not induce changes in Eucalyptus grandis leaves that alter the effect of constitutive defences on larvae of a specialist herbivore. Oecologia 156:847–859CrossRefGoogle Scholar
  16. Hol WHG, van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. J Chem Ecol 28:1763–1772CrossRefGoogle Scholar
  17. Hung CF, Prapaipong H, Berenbaum MR, Schuler MA (1995) Differential induction of cytochrome P450 transcripts in Papilio polyxenes by linear and angular furanocoumarins. Insect Biochem Mol Biol 25:89–99CrossRefGoogle Scholar
  18. Joosten L, Mulder PPJ, Klinkhamer PGL, van Veen JA (2009) Soil-borne microorganisms and soil-type affect pyrrolizidine alkaloids in Jacobaea vulgaris. Plant Soil 325:133–143CrossRefGoogle Scholar
  19. Karban R, Baldwin IT (2007) Induced responses to herbivory. The university of Chicago Press, ChicagoGoogle Scholar
  20. Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M, Seo S, Mitsuhara I (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Interact 6:221–230CrossRefGoogle Scholar
  21. Kirk H, Macel M, Klinkhamer PGL, Vrieling K (2004) Natural hybridization between Senecio jacobaea and Senecio aquaticus: molecular and chemical evidence. Mol Ecol 13:2267–2274CrossRefGoogle Scholar
  22. Kostenko O, Mulder PPJ, Bezemer TM (2013) Effects of root herbivory on pyrrolizidine alkaloid content and aboveground plant-herbivore-parasitoid interactions in Jacobaea vulgaris. J Chem Ecol 39:109–119CrossRefGoogle Scholar
  23. Kowalchuk G, Hol W, van Veen J (2006) Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biol Biochem 38:2852–2859CrossRefGoogle Scholar
  24. Ku KM, Jeffery EH, Juvik JA (2006) Exogenous methyl jasmonate treatment increases glucosinolate biosynthesis and quinone reductase activity in kale leaf tissue. PLoS One 9:e103407CrossRefGoogle Scholar
  25. Largia MJV, Pothiraj G, Shilpha J, Ramesh M (2015) Methyl jasmonate and salicylic acid synergism enhances bacoside A content in shoot cultures of Bacopa monnieri (L.). Plant Cell Tissue Organ Cult 122:9–20CrossRefGoogle Scholar
  26. Liang YS, Choi YH, Kim HK, Linthorst HJ, Verpoorte R (2006) Metabolomic analysis of methyl jasmonate treated Brassica rapa leaves by 2-dimensional NMR spectroscopy. Phytochemistry 67:2503–2511CrossRefGoogle Scholar
  27. Liu X, Klinkhamer PGL, Vrieling K (2017) The effect of structurally related metabolites on insect herbivores: a case study on pyrrolizidine alkaloids and western flower thrips. Phytochemistry 138:93–103CrossRefGoogle Scholar
  28. Macel M (2011) Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochem Rev 10:75–82CrossRefGoogle Scholar
  29. Macel M, Klinkhamer PGL (2010) Chemotype of Senecio jacobaea affects damage by pathogens and insect herbivores in the field. Evol Ecol 24:237–250CrossRefGoogle Scholar
  30. Macel M, Klinkhamer PGL, Vrieling K, van der Meijden E (2002) Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133:541–550CrossRefGoogle Scholar
  31. Macel M, Vrieling K, Klinkhamer PGL (2004) Variation in pyrrolizidine alkaloid patterns of Senecio jacobaea. Phytochemistry 65:865–873CrossRefGoogle Scholar
  32. Macel M, Bruinsma M, Dijkstra SM, Ooijendijk T, Niemeyer HM, Klinkhamer PGL (2005) Differences in effects of pyrrolizidine alkaloids on five generalist insect herbivore species. J Chem Ecol 31:1493–1508CrossRefGoogle Scholar
  33. McLaren D, Ireson J, Kwong R (2000) Biological control of ragwort (Senecio jacobaea L.) in Australia. Proceedings of the X international symposium on biological control of weeds, pp 67–79Google Scholar
  34. Miller B, Madilao LL, Ralph S, Bohlmann J (2005) Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol 137:369–382CrossRefGoogle Scholar
  35. Niemüller D, Reimann A, Ober D (2012) Distinct cell-specific expression of homospermidine synthase involved in pyrrolizidine alkaloid biosynthesis in three species of the Boraginales. Plant Physiol 159:920–929CrossRefGoogle Scholar
  36. Nuringtyas TR, Verpoorte R, Klinkhamer PGL, van Oers MM, Leiss KA (2014) Toxicity of pyrrolizidine alkaloids to Spodoptera exigua using insect cell lines and injection bioassays. J Chem Ecol 40:609–616CrossRefGoogle Scholar
  37. Ober D, Kaltenegger E (2009) Pyrrolizidine alkaloid biosynthesis, evolution of a pathway in plant secondary metabolism. Phytochemistry 70:1687–1695CrossRefGoogle Scholar
  38. Pelser PB, Gravendeel B, van der Meijden R (2003) Phylogeny reconstruction in the gap between too little and too much divergence: the closest relatives of Senecio jacobaea (Asteraceae) according to DNA sequences and AFLPs. Mol Phylogenet Evol 29:613–628CrossRefGoogle Scholar
  39. Rinkel J, Dickschat JS (2015) Recent highlights in biosynthesis research using stable isotopes. Beilstein J Org Chem 11:2493–2508CrossRefGoogle Scholar
  40. Singh P (1983) A general purpose laboratory diet mixture for rearing insects. Int J Trop Insect Sci 4:357–362CrossRefGoogle Scholar
  41. Traw BM, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133:1367–1375CrossRefGoogle Scholar
  42. Traw BM, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532CrossRefGoogle Scholar
  43. Trigo JR (2011) Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10:83–98CrossRefGoogle Scholar
  44. van Dam NM, Oomen MWAT (2008) Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signal Behav 3:91–98CrossRefGoogle Scholar
  45. van Dam NM, Vrieling K (1994) Genetic variation in constitutive and inducible pyrrolizidine alkaloid levels in Cynoglossum officinale L. Oecologia 99:374–378CrossRefGoogle Scholar
  46. van Dam NM, Witjes L, Svatoš A (2004) Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytol 161:801–810CrossRefGoogle Scholar
  47. Vrieling K, de Vos H, van Wijk CA (1993) Genetic analysis of the concentrations of pyrrolizidine alkaloids in Senecio jacobaea. Phytochemistry 32:1141–1144CrossRefGoogle Scholar
  48. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216Google Scholar
  49. Wang P, Guo L, Jaini R, Klempien A, McCoy RM, Morgan JA, Dudareva N, Chapple C (2018) A 13C isotope labeling method for the measurement of lignin metabolic flux in Arabidopsis stems. Plant Methods 14:51CrossRefGoogle Scholar
  50. Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19CrossRefGoogle Scholar
  51. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Life SciencesNankai UniversityTianjinChina
  2. 2.Plant Ecology and Phytochemistry, Institute of BiologyLeiden UniversityLeidenThe Netherlands
  3. 3.RIKILT-Wageningen University & ResearchWageningenThe Netherlands

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