New roles for cis-jasmone as an insect semiochemical and in plant defense

Abstract

cis-jasmone, or (Z)-jasmone, is well known as a component of plant volatiles, and its release can be induced by damage, for example during insect herbivory. Using the olfactory system of the lettuce aphid to investigate volatiles from plants avoided by this insect, (Z)-jasmone was found to be electrophysiologically active and also to be repellent in laboratory choice tests. In field studies, repellency from traps was demonstrated for the damson-hop aphid, and with cereal aphids numbers were reduced in plots of winter wheat treated with (Z)-jasmone. In contrast, attractant activity was found in laboratory and wind tunnel tests for insects acting antagonistically to aphids, namely the seven-spot ladybird and an aphid parasitoid. When applied in the vapor phase to intact bean plants, (Z)-jasmone induced the production of volatile compounds, including the monoterpene (E)-beta-ocimene, which affect plant defense, for example by stimulating the activity of parasitic insects. These plants were more attractive to the aphid parasitoid in the wind tunnel when tested 48 h after exposure to (Z)-jasmone had ceased. This possible signaling role of (Z)-jasmone is qualitatively different from that of the biosynthetically related methyl jasmonate and gives a long-lasting effect after removal of the stimulus. Differential display was used to compare mRNA populations in bean leaves exposed to the vapor of (Z)-jasmone and methyl jasmonate. One differentially displayed fragment was cloned and shown by Northern blotting to be up-regulated in leaf tissue by (Z)-jasmone. This sequence was identified by homology as being derived from a gene encoding an alpha-tubulin isoform.

Figure 1

Coupled GC-EAG with summer morph of the lettuce aphid, N. ribis-nigri. (Upper) GC of volatiles from black currant, R. nigrum. (Lower) Simultaneous EAG response of N. ribis-nigri. Compounds eliciting major EAG responses (in order of elution) are: 1, 5-methylfurfural; 2, 1-octen-3-ol; 3, β-pinene; 4, chrysanthenone; 5, methyl salicylate; 6, (Z)-jasmone; 7, caryophyllene; 8, (E)-β-farnesene. A = peak from (Z)-jasmone.

Figure 2

SCR with summer morph of the lettuce aphid, N. ribis-nigri. (a) Response of an olfactory cell in the proximal primary rhinarium (fifth antennal segment) to (Z)-jasmone (1 μg). Stimulus applied over 2 sec; beginning and end of stimulus period are marked as X and Y, respectively. (b) Dose–response of a single olfactory cell to (Z)-jasmone and methyl jasmonate. Each point is the mean of two stimulations on the same preparation.

Figure 3

Levels of (E)-β-ocimene produced by bean plants, V. faba, during 48-h entrainments after 24 h exposure to (Z)-jasmone (100 μg⋅liter^-1 in air).

Figure 4

Differential expression of a gene-specific sequence (D251) in V. faba plants. Total RNA was isolated from stem or leaf tissue of plants exposed to air, methyl jasmonate, or (Z)-jasmone. Ten micrograms RNA per sample was loaded and separated on a formaldehyde gel (A). The samples then were transferred to a nylon membrane and probed with the D251 sequence (B). Lane 1 = air treatment (control); lane 2 = (Z)-jasmone treatment; lane 3 = methyl jasmonate treatment. In the case of RNA isolated from leaf tissue, only (Z)-jasmone treatment results in up-regulation.

Figure 5

Sequence comparison between the deduced amino acid sequence of the coding sequence of D251 and α-tubulin isoforms present on GenBank. Sequences shown are A. thaliana α-tubulin genes A1, A2, A4, A5, A6 and P. sativum α-tubulin A1.