Color morphology of Diaphorina citri influences interactions with its bacterial endosymbionts and 'Candidatus Liberibacter asiaticus'

Authors: HOSSEINZADEH, SAEED - Boyce Thompson Institute; Ramsey, John - John; MANN, MARINA - Boyce Thompson Institute; BENNETT, LILY - Haverford College; Hunter, Wayne; SHAMS-BAKHSH, MASOUD - Tarbiat Modares University; Hall, David; Heck, Michelle

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/24/2019
Publication Date: 5/16/2019
Citation: Hosseinzadeh, S., Ramsey, J.S., Mann, M., Bennett, L., Hunter, W.B., Shams-Bakhsh, M., Hall, D.G., Heck, M.L. 2019. Hemocyanin protein expression is correlated with color morphology and immunity to ‘Candidatus Liberibacter asiaticus’ in the Huanglongbing insect vector, Diaphorina citri. PLoS One. 14(5):e0216599. https://doi.org/10.1371/journal.pone.0216599.
DOI: https://doi.org/10.1371/journal.pone.0216599

Interpretive Summary: The Asian citrus psyllid (ACP, Diaphorina citri) is the insect vector responsible for the spread of citrus greening disease. Within a population of ACP, not all insects can spread CLas (Candidatus Liberibacter asiaticus). We have associated some of this variation with an immunity protein produced by the ACP. This protein, hemocyanin, contains copper for oxygen binding, conferring a blue color to the ACP abdomens. One may consider it the insect equivalent of animal hemoglobin. We report here that blue insects have higher levels of hemocyanin and copper, and lower levels of CLas, than non-blue insects from the same population. Citrus plants inoculated with CLas from non-blue ACP developed higher levels of CLas as compared to plants inoculated with blue ACP. Targeted control strategies are being developed based on this enhanced understanding of insect immunity and pathogen transmission within the insect. The connection between ACP immune response against CLas and blue abdominal coloration suggests the value of using this visual marker as a data point in citrus grove insect surveillance.

Technical Abstract: The Asian citrus psyllid (ACP, Diaphorina citri), is an economically important pest of citrus and a vector of ‘Candidatus Liberibacter asiaticus’ (CLas), the bacterial pathogen associated with Huanglongbing, (HLB, or citrus greening). HLB is the most severe disease of citrus worldwide. We previously found that hemocyanin, a copper and oxygen binding protein, is highly induced in insects reared on CLas infected trees. Here we show that in the ACP, hemocyanin protein expression and blue abdominal coloration are inversely proportional to CLas titer and transmission ability. Blue insects have higher levels of hemocyanin protein, and a lower level of CLas in their bodies after acquisition, compared to their grey and yellow conspecifics. Accordingly, the CLas titer in citrus leaves inoculated by yellow or grey insects is 6-fold higher than in leaves inoculated by blue insects. A greater proportion of blue insects can be observed on CLas infected trees as compared to healthy trees in a single genetic population of ACP, suggesting some degree of plasticity in the hemocyanin response dependent on the presence of CLas infection in the plant. While it is certain that other ACP proteins are involved in the immune response of adult psyllids to CLas, these data provide support for the hypothesis that hemocyanin is a key molecular interface in a vector-pathogen tug-of-war, where CLas is a pathogen of the adult insect as well as the citrus tree.