Engineered Orange Ectopically Expressing the Arabidopsis β-Caryophyllene Synthase Is Not Attractive to Diaphorina citri, the Vector of the Bacterial Pathogen Associated to Huanglongbing

Abstract

Huanglongbing (HLB) is a destructive disease, associated with psyllid-transmitted phloem-restricted pathogenic bacteria, which is seriously endangering citriculture worldwide. It affects all citrus species and cultivars regardless of the rootstock used, and despite intensive research in the last decades, there is no effective cure to control either the bacterial species (Candidatus Liberibacter spp.) or their insect vectors (Diaphorina citri and Trioza erytreae). Currently, the best attempts to manage HLB are based on three approaches: (i) reducing the psyllid population by intensive insecticide treatments; (ii) reducing inoculum sources by removing infected trees, and (iii) using nursery-certified healthy plants for replanting. The economic losses caused by HLB (decreased fruit quality, reduced yield, and tree destruction) and the huge environmental costs of disease management seriously threaten the sustainability of the citrus industry in affected regions. Here, we have generated genetically modified sweet orange lines to constitutively emit (E)-β-caryophyllene, a sesquiterpene repellent to D. citri, the main HLB psyllid vector. We demonstrate that this alteration in volatile emission affects behavioral responses of the psyllid in olfactometric and no-choice assays, making them repellent/less attractant to the HLB vector, opening a new alternative for possible HLB control in the field.

Repellent Activity of Clove Essential Oil Volatiles and Development of Nanofiber-Based Dispensers against Pear Psyllids (Hemiptera: Psyllidae)

“…Since the produced fibers did not contain these compounds, they would not be as effective against this species in the field. β-caryophyllene has already been described as a repellent against Diaphorina citri [ 56 , 57 ]. The repellent effect of β-caryophyllene together with eugenyl acetate against the pear psyllid C. pyri has been demonstrated in our tests, but not as a single compound; however, it could probably have a repellent effect in a dose-dependent matter.…”

Insect pest management in the age of synthetic biology

“…Overexpression of an endogenous terpene synthase in rice (Os TPS46 ) led to overproduction of ( E )‐β‐farnesene and limonene, deterring feeding by the bird cherry‐oat aphid, Rhopalosiphum padi (Sun et al ., 2017 ), and tobacco plants genetically engineered to produce ( E )‐β‐farnesene synthase from peppermint showed decreased levels of aphid infestation (Yu et al ., 2013 ). Overexpression of ( E )‐β‐caryophyllene, another volatile sesquiterpene found in plants and emitted by some insects as a semiochemical (El‐Sayed, 2021 ), in A. thaliana repelled the vector of citrus disease Huanglongbing, Diaphorina citri (Alquézar et al ., 2017 ) and expression of the same gene in sweet orange produced similar effects (Alquézar et al ., 2021 ). Lectins, common in many plants, bind to carbohydrate structures in the midguts of phytophagous insects causing disruption of the digestive system.…”

Metabolic engineering in woody plants: challenges, advances, and opportunities

“…Overexpressing the Arabidopsis β -caryophyllene synthase gene in sweet orange leaves caused large emissions of a VOC β-caryophyllene. As β-caryophyllene functions as a repellent of Diaphorina citri , the transgenic orange plants showed reduced attraction to D. citri , an insect vector of the notorious crop disease “Huanglongbing”, in olfactometric behavioral assays and the choice behavioral test, demonstrating the potential of this approach for controlling Huanglongbing (Alquézar et al 2021 ).…”