Phytoene desaturase-silenced citrus as a trap crop with multiple cues to attract Diaphorina citri, the vector of Huanglongbing

Authors: KILLINY, NABIL - University Of Florida; NEHELA, YASSER - Tanta University; George, Justin; RASHIDI, MAHNAZ - University Of Florida; STELINSKI, LUKASZ - University Of Florida; Lapointe, Stephen

Submitted to: Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/24/2021
Publication Date: 4/29/2021
Citation: Killiny, N., Nehela, Y., George, J., Rashidi, M., Stelinski, L.L., Lapointe, S.L. 2021. Phytoene desaturase-silenced citrus as a trap crop with multiple cues to attract Diaphorina citri, the vector of Huanglongbing. Plant Science. 308:110930. https://doi.org/10.1016/j.plantsci.2021.110930.
DOI: https://doi.org/10.1016/j.plantsci.2021.110930

Interpretive Summary: Asian citrus psyllid (Diaphorina Citri Kuwayama) (Hemiptera: Liviidae) is the major vector of Huanglongbing (HLB) disease pathogen that causes the most destructive citrus disease in the world. Unfortunately, HLB has no cure and management relies on insecticides to reduce populations of the vector, D. citri. We propose an attract-and-kill strategy using a trap crop as an alternative to vector control to reduce transmission of the pathogen, ‘Candidatus Liberibacter asiaticus’. We evaluated vector response to phytoene desaturase-silenced citrus trees using virus-induced gene silencing technology. Citrus tristeza virus was used to produce a phytoene desaturase-silenced citrus (CTV-tPDS) that expresses visual, olfactory, and gustatory cues to attract D. citri. We found that D. citri were more attracted to CTV-tPDS plants with noticeably better fecundity and overall population fitness than on control plants. Moreover, rearing D. citri on CTV-tPDS plants significantly increased their survival probability compared with those reared on control plants. CTV-tPDS plants possessed reduced content of both carotenoid and chlorophyll pigments resulting in a consistent photobleached phenotype on citrus leaves which provided a sufficient close-range visual attractant to stimulate D. citri landing. Finally, CTV-tPDS plants exhibited both enhanced phloem sap chemical composition and leaf metabolite profile which offered appropriate gustatory cues that influenced probing/feeding behavior. We believe that introducing CTV-tPDS plants (as a trap crop) to D. citri-infested orchards will attract and congregate psyllids to facilitate their removal from the target crop with insecticides or by other means. Moreover, it is an eco-friendly strategy because it should partially reduce the input of chemical insecticides ameliorating the indirect cost of HLB infection.

Technical Abstract: Huanglongbing (HLB) is one of the most destructive diseases in citrus worldwide. Unfortunately, HLB has no cure and management relies on insecticides to reduce populations of the vector, Diaphorina citri Kuwayama (Hemiptera: Liviidae). We propose an attract-and-kill strategy using a trap crop as an alternative to vector control to reduce transmission of the pathogen, ‘Candidatus Liberibacter asiaticus’. We evaluated vector response to phytoene desaturase-silenced citrus trees using virus-induced gene silencing technology. Citrus tristeza virus was used to produce a phytoene desaturase-silenced citrus (CTV-tPDS) that expresses visual, olfactory, and gustatory cues to attract D. citri. We found that D. citri were more attracted to CTV-tPDS plants with noticeably better fecundity and overall population fitness than on control plants. Moreover, rearing D. citri on CTV-tPDS plants significantly increased their survival probability compared with those reared on control plants. CTV-tPDS plants possessed reduced content of both carotenoid and chlorophyll pigments resulting in a consistent photobleached phenotype on citrus leaves which provided a sufficient close-range visual attractant to stimulate D. citri landing. Additionally, CTV-tPDS plants exhibited an enriched profile of volatile organic compounds (VOCs), which offered adequate olfactory cues to attract psyllid from distance. Finally, CTV-tPDS plants exhibited both enhanced phloem sap chemical composition and leaf metabolite profile which offered appropriate gustatory cues that influenced probing/feeding behavior. We believe that introducing CTV-tPDS plants (as a trap crop) to D. citri-infested orchards will attract and congregate psyllids to facilitate their removal from the target crop with insecticides or by other means. This new strategy could be deployed relatively quickly and economically to HLB-impacted citrus industries. Moreover, it is an eco-friendly strategy because it should partially reduce the input of chemical insecticides ameliorating the indirect cost of HLB infection.