Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

Abstract

Herbivore-induced plant defences influence the behaviour of insects associated with the plant. For biting-chewing herbivores the octadecanoid signal-transduction pathway has been suggested to play a key role in induced plant defence. To test this hypothesis in our plant-herbivore-parasitoid tritrophic system, we used phenidone, an inhibitor of the enzyme lipoxygenase (LOX), that catalyses the initial step in the octadecanoid pathway. Phenidone treatment of Brussels sprouts plants reduced the accumulation of internal signalling compounds in the octadecanoid pathway downstream of the step catalysed by LOX, i.e. 12-oxo-phytodienoic acid (OPDA) and jasmonic acid. The attraction of Cotesia glomerata parasitoids to host-infested plants was significantly reduced by phenidone treatment. The three herbivores investigated, i.e. the specialists Plutella xylostella, Pieris brassicae and Pieris rapae, showed different oviposition preferences for intact and infested plants, and for two species their preference for either intact or infested plants was shown to be LOX dependent. Our results show that phenidone inhibits the LOX-dependent defence response of the plant and that this inhibition can influence the behaviour of members of the associated insect community.

Fig. 1

Representation of the octadecanoid pathway from α-linolenic acid (after Creelman and Mulpuri ; D’Auria et al. 2007)

Fig. 2

Oviposition preference of Pieris brassicae on a P. brassicae-infested versus uninfested (control) leaves, b phenidone-treated leaves with or without P. brassicae, c P. brassicae-infested leaves with or without phenidone. The thick line indicates the median, the box represents the interquartile range from first to third quartile. **P < 0.01. n.s. Not significant (Wilcoxon matched pair signed rank test)

Fig. 3

Oviposition preference of Plutella xylostella on a Pieris rapae-infested versus uninfested (control) leaves, b phenidone-treated leaves with or without Pieris rapae, c Pieris rapae-infested leaves with or without phenidone. The thick line indicates the median, the box represents the interquartile range from first to third quartile. **P < 0.01, ***P < 0.001 (Wilcoxon matched pair signed rank test)

Fig. 4

Attraction of Cotesia glomerata to plants sprayed with phenidone (phen) or sprayed with a control solution, with or without infestation with Pieris brassicae (PB). Numbers to the left of the bars indicate the total number of parasitoids tested, numbers in parentheses indicate the number of parasitoids that landed on a plant. **P < 0.01, ***P < 0.001 (binomial test)

Fig. 5

Effect of phen treatment and caterpillar infestation on a 12-oxo-phytodienoic acid (OPDA), and b jasmonic acid levels in Pieris rapae-infested (PR), PB-infested, phen-treated P. rapae-infested (PR + phen) and phen-treated P. brassicae-infested (PB + phen) Brussels sprouts plants. Different letters indicate significant differences between treatments. For other abbreviations, see Fig. 4

Fig. 6

Multivariate data analysis of the volatile pattern of plants infested with PB, phen-treated PB-infested plants (PHEN + PB), and phen-treated intact plants (PHEN). Percentage variation explained in parentheses. The ellipse defines the Hotelling’s T ² confidence region (95%). a Score plot of principal component analysis (PCA), and b score plot of projection to latent structures-discriminant analysis (PLS-DA), and c loading plot of PLS-DA as based on the relative amounts of 20 volatile compounds from the differently treated Brussels sprouts plants. Compound identification numbers correspond to numbers in Table 1. For other abbreviations, see Fig. 4