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

A - Papers appearing in refereed journals

Birkett, M. A., Campbell, C. A. M., Chamberlain, K., Guerrieri, E., Hick, A. J., Martin, J. L., Matthes, M. C., Napier, J. A., Pettersson, J., Pickett, J. A., Poppy, G. M., Pow, E. M., Pye, B. J., Smart, L. E., Wadhams, G. H., Wadhams, L. J. and Woodcock, C. M. 2000. New roles for cis-jasmone as an insect semiochemical and in plant defense. Proceedings of the National Academy of Sciences of the United States of America - PNAS. 97 (16), pp. 9329-9334.

AuthorsBirkett, M. A., Campbell, C. A. M., Chamberlain, K., Guerrieri, E., Hick, A. J., Martin, J. L., Matthes, M. C., Napier, J. A., Pettersson, J., Pickett, J. A., Poppy, G. M., Pow, E. M., Pye, B. J., Smart, L. E., Wadhams, G. H., Wadhams, L. J. and Woodcock, C. M.
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)-β-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 α-tubulin isoform. Plants have evolved a variety of mechanisms to withstand the damage and stresses caused by pathogens and herbivorous animals, as well as by many abiotic factors. One such mechanism involves the emission of volatile compounds, either constitutively or as a result of biotic infestation or physical damage, which can affect pathogen development and the behavior of insect herbivores searching for a food source. A recent review by Agrawal and Karban (1) compares the benefits to the plant of constitutive gene expression and induced defense strategies. Constitutively produced plant volatiles play a role in attracting pollinators and seed-dispersing animals; in addition, they can repel a wide range of potential herbivores and attract a smaller number of pest species that have evolved to take advantage of these chemicals in finding food. Plant volatiles that are induced on damage to repel insect attack also may act as an indirect plant defense mechanism by attracting other insects that prey on or parasitize the herbivores. Such compounds also may act as signals between plants, whereby defense mechanisms are induced in undamaged plants in response to volatiles produced by neighboring infested plants, and specific volatiles, methyl salicylate and methyl jasmonate, have been implicated (2–5). Compounds containing six carbon atoms, e.g., (E)-2-hexenal, which are rapidly emitted from damaged or wounded plant tissue, also have recently been shown to induce the expression of defense-related genes in intact plants (6). The investigation of insect interactions with plant volatiles is now greatly facilitated by using sophisticated electrophysiological techniques, in particular gas chromatography (GC) coupled directly to neuronal or single-cell recording (SCR) from the olfactory organs of insects. Methyl salicylate, which was found to repel aphids (Homoptera: Aphididae) such as the black bean aphid, Aphis fabae, and cereal aphids including the grain aphid, Sitobion avenae, and also to inhibit attraction to their host plants (7, 8), originally was discovered to be an aphid signal by SCR on the antenna of the bird-cherry-oat aphid, Rhopalosiphum padi (7). More than 30 species of insects, both plant feeders and their natural enemies, from five orders subsequently have been found, by SCR and by recording from the whole antenna (electroantennography, or EAG), to possess olfactory receptors for this compound (C.M.W., unpublished work). Subsequently, Raskin's group (3) showed that methyl salicylate may act as an airborne plant signal mediating plant pathogen resistance. Following the successful use of the techniques outlined above, we began the investigation of other plant/aphid interactions, selecting plants that were nonhosts for certain aphid species or morphs. Ribes nigrum, the black currant (Saxifragaceae), which with other Ribes species is the winter (primary) host of the lettuce aphid, Nasonovia ribis-nigri, was studied as part of the investigation. This plant is attractive to the morphs of N. ribis-nigri produced in the autumn but is avoided by, and indeed repellent to, the spring and summer morphs, which are attracted to the summer (secondary) hosts such as lettuce, Lactuca sativa (Asteraceae). In this paper, we describe how cis-jasmone, or (Z)-jasmone, a component of flower volatiles also known to be induced on damage to plant vegetative tissue (9, 10), was located in the volatile profile of R. nigrum by coupled GC-EAG on the summer morph of N. ribis-nigri. (Z)-Jasmone was singled out from other electrophysiologically active compounds in the extract because of its clear biosynthetic association to the stress-induced jasmonic acid or octadecanoid pathway. The compound was shown to be repellent to this aphid in laboratory tests and the generality of its repellent activity for aphids was demonstrated in field trials with other species. In addition, the effects of (Z)-jasmone on two natural control agents of aphids, a predator, the seven-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae), and the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae), were determined. Finally, the bean plant Vicia faba (Fabaceae) was exposed to (Z)-jasmone in the vapor phase to investigate whether this compound affects insect behavior by altering the release of volatiles and gene expression by the plant.

KeywordsRRES175; 175_Entomology; 175_Plant sciences; 175_Biochemistry
Year of Publication2000
JournalProceedings of the National Academy of Sciences of the United States of America - PNAS
Journal citation97 (16), pp. 9329-9334
Digital Object Identifier (DOI)doi:10.1073/pnas.160241697
PubMed ID10900270
Open accessPublished as bronze (free) open access
Funder project or code437
415
Publisher's version
Publication dates
Online18 Jul 2000
Publication process dates
Accepted25 May 2000
PublisherNational Academy of Sciences
National Academy of Sciences of the United States of America
ISSN0027-8424

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