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Jasmonate-mediated induced volatiles in the American cranberry, Vaccinium macrocarpon: from gene expression to organismal interactions

Cesar R. Rodriguez-Saona, James Polashock, Edi A. Malo
Frontiers in plant science 2013 v.4 no. pp. 1-17
Araneae, Cicadellidae, Lymantria dispar, Sparganothis, Vaccinium macrocarpon, acetates, adults, biosynthesis, cranberries, diurnal variation, emissions, enzymes, gene expression, gene expression regulation, genes, herbivores, hormones, jasmonic acid, larvae, leaves, linalool, mechanical damage, methyl jasmonate, mortality, moths, natural enemies, odors, parasitic wasps, pest resistance, plant-insect relations, predator-prey relationships, progeny, sesquiterpenoids, sticky traps, volatile compounds
Jasmonates, i.e., jasmonic acid (JA) and methyl jasmonate (MeJA), are signaling hormones that regulate a large number of defense responses in plants which in turn affect the plants’ interactions with herbivores and their natural enemies. Here, we investigated the effect of jasmonates on the emission of volatiles in the American cranberry, Vaccinium macrocarpon, at different levels of biological organization from gene expression to organismal interactions. Plants were treated with exogenous 1 mM MeJA or JA and the up-regulation of key terpene biosynthesis genes, induction of volatiles, and effects on herbivores and herbivore natural enemies were measured. At the molecular level, of the eight genes targeted, four (BCS, LLS, NER1, and TPS21) responded dramatically to gypsy moth larval feeding, MeJA, and mechanical wounding, but to different degrees. The most dramatic changes in expression of BCS and TPS21were when treated with MeJA; these genes are in the sesquiterpenoid pathway and the enzymes encoded catalyze the production of ß-caryophyllene and a-humulene, respectively. Gypsy moth larval feeding and MeJA treated plants also had dramatically elevated expression of LLS and NER1 [LLS is in the monoterpenoid pathway and the encoded enzyme catalyzes the synthesis of linalool; NER1 is in the homoterpene biosynthesis pathway and the encoded enzyme catalyzes the synthesis of 4,8-dimethyl-1,3,7-nonatriene (DMNT)]. At the biochemical level, MeJA induced a complex blend of volatile compounds including linalool, DMNT, ß-caryophyllene, and a-humulene that differed from gypsy moth and mechanical damage, and followed a diurnal pattern of emission. At the organismal level, numbers of Sparganothis sulfureana moths were lower while numbers of parasitic wasps were higher on sticky traps near MeJA-treated cranberry plants than those near untreated plants. No effects were found for leafhoppers (herbivores) or predatory syrphids, spiders, and pirate bugs. Out of 11 leaf volatiles tested, (Z)-3-hexenyl acetate, linalool, and linalool oxide elicited strong antennal (EAG) responses from S. sulfureana, whereas sesquiterpenes elicited weak EAG responses. In addition, mortality of S. sulfureana larvae increased by about 43% in JA-treated cranberry plants as compared with untreated plants, indicating a relationship among adult preference, antennal sensitivity to plant odors, and offspring performance. This study highlights the role of the jasmonate-dependent defensive pathway in the emissions of herbivore-induced volatiles in cranberries and its importance in multi-trophic level interactions.