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

Authors: GUO, CHANG-FEI - Changqing Key Laboratory; Ahmed, Muhammad; OU, DA - South China Agricultural University; ZHANG, LI-HE - National Engineering Research Center For Information Technology In Agriculture; LU, ZI-TONG - Changqing Key Laboratory; SANG, WEN - South China Agricultural Univerisity; McKenzie, Cindy; Shatters, Robert - Bob; QIU, BAO-LI - Guangdong Testing Institute Of Product Quality Supervision

Submitted to: Communications Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/1/2021
Publication Date: 11/25/2021
Citation: Guo, C., Ahmed, M.Z., Ou, D., Zhang, L., Lu, Z., Sang, W., Mckenzie, C.L., Shatters, R.G., Qiu, B. 2021. A parasitoid vectors a plant pathogen, potentially diminishing the benefits it confers as a biological control agent. Communications Biology. https://doi.org/10.1038/s42003-021-02851-2.
DOI: https://doi.org/10.1038/s42003-021-02851-2

Interpretive Summary: Parasitoids are frequently used in biological control and integrated pest management strategies all over the world. We illustrate, for the first time, an unappreciated risk posed by the use of such control agents. Deployment of parasitoids has been promoted as a means of suppressing the vector pest, Asian citrus psyllid (ACP), which naturally transmits citrus greening disease (Huanglongbing) in citrus orchards. However, while controlling ACP, the parasitoid Tamarixia radiata can inadvertently vector the Huanglongbing pathogen (CLas) thus diminishing its biological control efficiency; particularly in orchards where CLas infected and uninfected asymptomatic citrus trees coexist. Our finding presents a new and significant caution to the strategy of implementing biological control using parasitic wasps.

Technical Abstract: Huanglongbing is a destructive disease of citrus, which is primarily transmitted by the insect vector, Asian citrus psyllid (ACP).Biological control of ACP is an environmentally sustainable alternative to chemical control allowing management of chemical resistance, and alleviates human health concerns associated with heavy reliance on synthetic pesticides. However, the rational application of biological control agents and their risk in ACP management have never been evaluated. Here, for the first time, we reported that parasitoids, Tamarixia radiata, the most dominant parasitoid of ACP, could vector the Huanglongbing pathogen Candidatus Liberibacter asiaticus (CLas) and transmit it horizontally during probing and checking between ACP nymphs. Results revealed that parasitoids acquire CLas from CLas-infected ACP nymphs, and carry it in the ovipositors of adult females. When probing or checking CLas negative ACP hosts, parasitoids enter CLas into the hemolymph of probed/checked ACP. If parasitized ACP nymphs survived the parasitism, CLas spread into the salivary glands of ACP host after proliferation. While the CLas-recipient ACP individuals develop into adults and move to healthy citrus plants, CLas is transmitted to citrus leaves during infected ACP feeding, completing the transmission circle of the pathogen from CLas-infected ACP to parasitoid, from parasitoid to CLas uninfected-ACP and from CLas-recipient ACP to-citrus plant. We illustrate, for the first time, an unappreciated risk posed by the use of such parasitoids. Deployment of parasitoids has been promoted as a means of suppressing the ACP population naturally to circumvent the spread of CLas in citrus orchards; however, by functioning as a vector for horizontal transmission of CLas among CLas-free ACP nymphs, Tamarixia radiata can inadvertently contribute to spreading CLas disease in citrus orchards and will thus exacerbate the problem, particularly in the orchards where CLas infected, and uninfected asymptomatic citrus trees coexist. Our finding presents a new and significant challenge to the practice of biological control.