β-caryophyllene emitted from a transgenic Arabidopsis or chemical dispenser repels Diaphorina citri, vector of Candidatus Liberibacters

Abstract

Production of citrus, the main fruit tree crop worldwide, is severely threatened by Huanglongbing (HLB), for which as yet a cure is not available. Spread of this bacterial disease in America and Asia is intimately connected with dispersal and feeding of the insect vector Diaphorina citri, oligophagous on rutaceous host plants. Effective control of this psyllid is an important component in successful HLB management programs. Volatiles released from the non-host guava have been shown to be repellent to the psyllid and to inhibit its response to citrus odour. By analysing VOC emission from guava we identified one volatile compound, (E)-β-caryophyllene, which at certain doses exerts a repellent effect on D. citri. Non-host plant rejection mediated by (E)-β-caryophyllene is demonstrated here by using Arabidopsis over-expression and knock-out lines. For the first time, results indicate that genetically engineered Arabidopsis plants with modified emission of VOCs can alter the behaviour of D. citri. This study shows that transgenic plants with an inherent ability to release (E)-β-caryophyllene can potentially be used in new protection strategies of citrus trees against HLB.

The role of volatiles in plant communication

“…As described above, the ubiquitous volatile terpene ( E )‐β‐caryophyllene repels a number of agriculturally important pests, including psyllids (Zhang et al ., ). Intercropping (with the ( E )‐β‐caryophyllene emitting guave) or possibly the application of ( E )‐β‐caryophyllene dispensers may provide solutions for this enormous agricultural problem (Mafra‐Neto et al ., ; Alquézar et al ., ) (Figure f).…”

“…(f) ( E )‐β‐caryophyllene repels HLB transmitting Diaphorina citri . Naturally ( E )‐β‐caryophyllene emitting plant species such as guave, the use of ( E )‐β‐caryophyllene dispensers and metabolic engineering of ( E )‐β‐caryophyllene production can potentially be used to protect citrus trees against HLB (Mafra‐Neto et al ., ; Alquézar et al ., ).…”

“…Both compounds were shown to protect the transgenic chrysanthemum against aphids due to their repellent and antifeedant activity, respectively. In an attempt to protect citrus against D. citri , the Arabidopsis ( E )‐β‐caryophyllene synthase was overexpressed in Arabidopsis (Alquézar et al ., ). Transgenic plants with enhanced ( E )‐β‐caryophyllene emission repelled D. citri suggesting that this strategy can potentially be used to protect citrus trees against HLB (Figure f).…”

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

“…Terpenoids are the most abundant compounds in plant volatiles. Sesquiterpenes and monoterpenes, such as (E)-α-bergamotene, (E)-β-caryophyllene, linalool, etc., are reported to generally have an effect on an insect's feeding orientation [94][95][96][97]. Many pathogens manipulate these chemical volatiles to alter their vectors' behaviors, especially insect-borne plant viruses, whose spread is highly reliant on insect vectors [2,98,99].…”

Temporal Decline in Pathogen-Mediated Release of Methyl Salicylate Associated With Decreasing Vector Preference for Infected Over Uninfected Plants

“…β-caryophyllene is the main constituent, with β-Ocimene, of a volatile blend known to increase capture of D. citri on yellow sticky traps (Patt and Setamou, 2010). However, when tested as an isolated compound in olfactometers, conflicting results were reported; Mann et al (2012) did not find any significant response associated to β-caryophyllene at 5 µg/µl, whereas Alquézar et al (2017) found it to repel D. citri at 1 and 10 µg/µl. In other systems, plant pathogen infection induced increased release of β-caryophyllene.…”