Parasitoid vectors a plant pathogen, potentially diminishing the benefits it confers as a biological control agent

Chang-Fei Guo,Li-He Zhang,Muhammad Z Ahmed,Wen Sang,Bao-Li Qiu,Robert G Shatters,Zi-Tong Lu,Da Ou,Cindy L Mckenzie

doi:10.1038/s42003-021-02851-2

Abstract

Huanglongbing (HLB) is a destructive disease of citrus primarily transmitted by the Asian citrus psyllid (ACP). Biocontrol of ACP is an environmentally sustainable alternative to chemicals. However, the risk of parasitoid rational application in ACP biocontrol has never been evaluated. Here we show, the dominant parasitoid of ACP, Tamarixia radiata, can acquire the HLB pathogen Candidatus Liberibacter asiaticus (CLas) and transmit it horizontally when probing ACP nymphs. If these ACP nymphs survive the probing, develop to adults and move to healthy plants, CLas can be transmitted to citrus leaves during feeding. We illustrate the formerly unrecognized risk that a parasitoid can potentially serve as a phoretic vector of the pathogen transmitted by its host, thus potentially diminishing some of the benefits it confers via biocontrol. Our findings present a significant caution to the strategy of using parasitoids in orchards with different infection status of insect-vectored pathogens.

Highlights

Huanglongbing (HLB) is a destructive disease of citrus primarily transmitted by the Asian citrus psyllid (ACP)
The question now is raised: is the increased percentage of the ACP population that is infected with Candidatus Liberibacter asiaticus (CLas), as a result of Tamarixia parasitoid transmission, significant enough to outweigh the benefit achieved by ACP population reduction through Tamarixia parasitism? our findings demonstrate that the potential negative effect of parasitoid-based horizontal transmission of plant pathogens should carefully appraise in other tritrophic systems such as plantaphid/whitefly/mealybug-parasitoid interactions
It has been proven that CLas pathogen can localize in different tissues and organs of T. radiata, after it is initially picked up during its development in CLas-infected ACP hosts

Summary

Introduction

Huanglongbing (HLB) is a destructive disease of citrus primarily transmitted by the Asian citrus psyllid (ACP). The dominant parasitoid of ACP, Tamarixia radiata, can acquire the HLB pathogen Candidatus Liberibacter asiaticus (CLas) and transmit it horizontally when probing ACP nymphs. If these ACP nymphs survive the probing, develop to adults and move to healthy plants, CLas can be transmitted to citrus leaves during feeding. T. radiata is a solitary, arrhenotokous ectoparasitoid, adult females of T. radiata feed on all the nymphal instars; they generally oviposit on the older nymphal instars (preferentially fourth and fifth instars)[13,14] This parasitoid has been used for the biological control of ACP in many regions of the world, and one field investigation has successfully demonstrated suppression in the ACP population in the natural environment without applying insecticides[12]. The question now is raised: is the increased percentage of the ACP population that is infected with CLas, as a result of Tamarixia parasitoid transmission, significant enough to outweigh the benefit achieved by ACP population reduction through Tamarixia parasitism? our findings demonstrate that the potential negative effect of parasitoid-based horizontal transmission of plant pathogens should carefully appraise in other tritrophic systems such as plantaphid/whitefly/mealybug-parasitoid interactions

Methods

Results

Conclusion