cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids

Abstract

It is of adaptive value for a plant to prepare its defenses when a threat is detected, and certain plant volatiles associated with insect damage, such as cis-jasmone (CJ), are known to switch-on defense metabolism. We used aphid and aphid parasitoid responses to Arabidopsis thaliana as a model system for studying gene expression and defense chemistry and its impact at different trophic levels. Differential responses to volatiles of induced Arabidopsis occurred for specialist and generalist insects: the generalist aphid, Myzus persicae, was repelled, whereas the specialist, Lipaphis erysimi, was attracted; the generalist aphid parasitoid Aphidius ervi was attracted, but the specialist parasitoid Diaeretiella rapae was not affected. A. ervi also spent longer foraging on induced plants than on untreated ones. Transcriptomic analyses of CJ-induced Arabidopsis plants revealed that a limited number of genes, including a gene for a cytochrome P450, CYP81D11, were strongly up-regulated in the treated plants. We examined transgenic Arabidopsis lines constitutively overexpressing this gene in bioassays and found insect responses similar to those obtained for wild-type plants induced with CJ, indicating the importance of this gene in the CJ-activated defense response. Genes involved in glucosinolate biosynthesis and catabolism are unaffected by CJ and, because these genes relate to interactions with herbivores and parasitoids specific to this family of plants (Brassicaceae), this finding may explain the differences in behavioral response of specialist and generalist insects.

Fig. 1.

Olfactometer responses of M. persicae (A), L. erysimi (B), and A. ervi (C). Corrected responses are shown (mean time spent in the control arms was subtracted from time spent in the treated arm for each replicate). Asterisks indicate where time spent in the treated arm was significantly different from time spent in the control arm (P < 0.05).

Fig. 2.

Foraging bioassay with A. ervi on CJ-treated Arabidopsis (A), A. ervi on CYP81D11-transformed Arabidopsis (B), and D. rapae on CJ-treated Arabidopsis (C). Asterisks indicate where treated and control responses were significantly different (P < 0.05).

Fig. 3.

Northern blotting analysis of CYP81D11 (At3g28740) expression by Arabidopsis wild-type and overexpressing plants. (A) Wild-type plants were exposed to CJ or methyl jasmonate for 20 h. RNA was subsequently extracted from leaves, and At3g28740 expression was analyzed by Northern blotting. (B) Tissue-specific expression of At3g28740 in Arabidopsis wild-type after ± exposure to CJ for 20 h. (C) Transgenic Arabidopsis lines constitutively overexpressing CYP81D11 (At3g28740) confirmed by Northern blotting. RNA was isolated from rosette leaves from homozygous T₃ plants used in subsequent bioassays.

Fig. 4.

GC-EAG with CYP81D11-induced Arabidopsis and A. ervi. Upper trace, response of antenna; lower trace, FID response. Electrophysiologically active peaks are marked with arrows. Tentative identifications based on retention indices and GC-MS: (1) (E)-2-pentenal, (2) (Z)-3-hexenal, (3) hexanal, (4) unidentified, (5) ethylbenzene. Tentative identifications based on retention index only, because of the small amount of material: (6) benzaldehyde/α-pinene, (7) 4-pentyl isothiocyanate/(E)-2-octen-1-ol, (8) unknown, (9) benzathiazole, (10) α-cubebene, (11) isolongifolene/bourbonene, (12) unidentified, (13) 2-tridecanone/germacrene D, (14) 4,8,12-trimethyl-(E,E)-trideca-1,3,7,11-tetraene, (15) unknown.