Enhanced β-ionone Emission in Arabidopsis Over-expressing <I>AtCCD1</I> Reduces Feeding Damage <I>in vivo</I> by the Crucifer Flea Beetle

Abstract

Plant carotenoid derived β-ionone has been shown to have diverse biological effects on some insect herbivores and herbivore parasitoids. In this study, Arabidopsis transgenic plants over-expressing a carotenoid cleavage dioxygenase1 gene (AtCCD1) were generated to test whether β-ionone emissions could be enhanced and used to control feeding by the crucifer flea beetle (Phyllotreta cruciferae Goeze). The transgenic plants exhibited a morphological phenotype indistinguishable from the wild type (WT) control over their complete life cycle. Gas chromatography and mass spectrometry analyses of headspace volatiles collected from 6-wk-old intact flowering plants revealed substantially enhanced β-ionone emission from transgenic plants compared with WT, but no β-ionone enhancement occurred at a young vegetative stage (4-wk-old seedlings). Bioassays in an enclosed environment showed that AtCCD1 over-expression resulted in ≍50% less leaf area damage by flea beetles on transgenic plants compared with WT plants. The mean number of damaged transgenic leaves per plant also was significantly lower in transgenic plants (P<0.05). Our results indicate that AtCCD1 over-expression and induced β-ionone emission might find application in the control of pests for Brassica crops grown in greenhouse operations. Potentially, β-ionone also could be used on crops grown in open-air ecosystems if this allomone is released in sufficient quantities to discourage herbivore foragers.

Synthesis and Function of Apocarotenoid Signals in Plants

“…Carotenoid leakage from plastids might also occur during insect attack, as suggested by Vogel [24], with carotenoids then cleaved to produce insect-repellent compounds. This theory concurs with the observation that CCD1 overexpression can reduce crucifer beetle attack [93]. A similar mechanism may help mitigate pathogen attack since many apocarotenoids seem to possess antimicrobial and antifungal properties [94].…”

UGT709G1: a novel uridine diphosphate glycosyltransferase involved in the biosynthesis of picrocrocin, the precursor of safranal in saffron (Crocus sativus)

“…Other apocarotenoid volatiles, such as β‐ionone, pseudoionone, and geranylacetone, are important contributors to flower‐scent perception by pollinators (Cobbs et al ., ); notably, all these compounds are also emitted by saffron stigmas (Moraga et al ., ). In addition, apocarotenoids have been shown to be strong deterrents of phytophagous insects (Wei et al ., ; Furstenberg‐Hagg et al ., ). Overall, this evidence suggests that the high level of picrocrocin in stigma tissues might confer an ecological advantage to saffron due to its bitter taste, as a defense mechanism against predators.…”

Carotenoid oxidation products as stress signals in plants

“…β–Ionone and β–cyclocitral were also reported to act as feeding deterrents of various herbivorous insects (Wang et al ., ; Gruber et al ., ; Nyalala et al ., ). Transgenic Arabidopsis plants overexpressing AtCCD1 exhibited enhanced β–ionone emission compared with the wild type (Wei et al ., ). Interestingly, the transgenics showed 50% less leaf area damage by flea beetles, confirming the beneficial effect of high β–ionone concentrations against herbivorous insects.…”