Methyl Jasmonate Changes the Composition and Distribution Rather than the Concentration of Defence Compounds: a Study on Pyrrolizidine Alkaloids
Tóm tắt
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.
Tài liệu tham khảo
Berenbaum MR, Nitao JK, Zangerl AR (1991) Adaptive significance of furanocoumarin diversity in Pastinaca sativa (Apiaceae). J Chem Ecol 17:207–215
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. https://doi.org/10.1007/s10886-006-9245-2
Chen H, Jones AD, Howe GA (2006) Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Lett 580:2540–2546
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 192:1010–1023
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 37:1071–1080
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 39:430–437
Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378
Gershenzon J, McConkey ME, Croteau RB (2000) Regulation of monoterpene accumulation in leaves of peppermint. Plant Physiol 122:205–214
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
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 89:2389–2393
Hartmann T (1999) Chemical ecology of pyrrolizidine alkaloids. Planta 207:483–495
Hartmann T, Dierich B (1998) Chemical diversity and variation of pyrrolizidine alkaloids of the senecionine type: biological need or coincidence? Planta 206:443–451
Hartmann T, Toppel G (1987) Senecionine N-oxide, the primary product of pyrrolizidine alkaloid biosynthesis in root cultures of Senecio vulgaris. Phytochemistry 26:1639–1643
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 177:98–107
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 156:847–859
Hol WHG, van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. J Chem Ecol 28:1763–1772
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 25:89–99
Joosten L, Mulder PPJ, Klinkhamer PGL, van Veen JA (2009) Soil-borne microorganisms and soil-type affect pyrrolizidine alkaloids in Jacobaea vulgaris. Plant Soil 325:133–143
Karban R, Baldwin IT (2007) Induced responses to herbivory. The university of Chicago Press, Chicago
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 6:221–230
Kirk H, Macel M, Klinkhamer PGL, Vrieling K (2004) Natural hybridization between Senecio jacobaea and Senecio aquaticus: molecular and chemical evidence. Mol Ecol 13:2267–2274
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 39:109–119
Kowalchuk G, Hol W, van Veen J (2006) Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biol Biochem 38:2852–2859
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:e103407
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 122:9–20
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 67:2503–2511
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 138:93–103
Macel M (2011) Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochem Rev 10:75–82
Macel M, Klinkhamer PGL (2010) Chemotype of Senecio jacobaea affects damage by pathogens and insect herbivores in the field. Evol Ecol 24:237–250
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 133:541–550
Macel M, Vrieling K, Klinkhamer PGL (2004) Variation in pyrrolizidine alkaloid patterns of Senecio jacobaea. Phytochemistry 65:865–873
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 31:1493–1508
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 67–79
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 137:369–382
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 159:920–929
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 40:609–616
Ober D, Kaltenegger E (2009) Pyrrolizidine alkaloid biosynthesis, evolution of a pathway in plant secondary metabolism. Phytochemistry 70:1687–1695
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 29:613–628
Rinkel J, Dickschat JS (2015) Recent highlights in biosynthesis research using stable isotopes. Beilstein J Org Chem 11:2493–2508
Singh P (1983) A general purpose laboratory diet mixture for rearing insects. Int J Trop Insect Sci 4:357–362
Traw BM, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133:1367–1375
Traw BM, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532
Trigo JR (2011) Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10:83–98
van Dam NM, Oomen MWAT (2008) Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signal Behav 3:91–98
van Dam NM, Vrieling K (1994) Genetic variation in constitutive and inducible pyrrolizidine alkaloid levels in Cynoglossum officinale L. Oecologia 99:374–378
van Dam NM, Witjes L, Svatoš A (2004) Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytol 161:801–810
Vrieling K, de Vos H, van Wijk CA (1993) Genetic analysis of the concentrations of pyrrolizidine alkaloids in Senecio jacobaea. Phytochemistry 32:1141–1144
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216
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 14:51
Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333