Development on Citrus medica infected with ‘Candidatus Liberibacter asiaticus’ has sex-specific and -nonspecific impacts on adult Diaphorina citri and its endosymbionts

Authors: COATES, LAURYNNE - University Of California, Davis; MAHONEY, JACLYN - (NCE, CECR)networks Of Centres Of Exellence Of Canada, Centres Of Excellence For Commercilization A; Ramsey, John - John; WARICK, ERICAROSE - University Of Florida; JOHNSON, RICHARD - University Of Washington; MACCOSS, MICHAEL - University Of Washington; Krasnoff, Stuart; Howe, Kevin; Moulton, Kathryn; SAHA, SURYA - Boyce Thompson Institute; MUELLER, LUKAS - Boyce Thompson Institute; Hall, David; Shatters, Robert - Bob; Heck, Michelle; SLUPSKY, CAROLYN - University Of California, Davis

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/14/2020
Publication Date: 10/6/2020
Citation: Coates, L.C., Mahoney, J., Ramsey, J.S., Warick, E., Johnson, R., Maccoss, M., Krasnoff, S., Howe, K.J., Moulton, K.M., Saha, S., Mueller, L., Hall, D.G., Shatters, R.G., Heck, M.L., Slupsky, C. 2020. Development on Citrus medica infected with ‘Candidatus Liberibacter asiaticus’ has sex-specific and -nonspecific impacts on adult Diaphorina citri and its endosymbionts. PLOS ONE. 15(1):e0239771. https://doi.org/10.1371/journal.pone.0239771.
DOI: https://doi.org/10.1371/journal.pone.0239771

Interpretive Summary: Huanglongbing (HLB), also referred to as citrus greening disease, is the most serious disease of citrus world-wide. In the USA, HLB in citrus is associated with plant infection by a bacterium that is spread by an invasive tiny, sap-sucking insect vector called the Asian citrus psyllid. Current management strategies that rely on insect vector control using pesticides are ineffective at controlling the spread of HLB in groves. An alternative strategy relies on blocking tree-to-tree psyllid transmission of the bacterium. To better understand how the psyllid vector spreads the HLB bacterium, university partners together with USDA ARS researchers studied the effects of infected trees on male and female insects. Insects were reared on healthy or HLB-infected citrus and various molecules were quantified, including mRNA, proteins, metabolites, beneficial bacterial partners of the insect, and the HLB bacterium. Despite the fact that the HLB bacterium was at similar levels in male and female insects, the different sexes showed dramatic differences in their physiological response to HLB-infected trees. These findings indicate that novel strategies aimed at transmission blocking to stop the spread of HLB must be tested on both male and female insects separately to optimize field delivery strategies.

Technical Abstract: Huanglongbing (HLB) is a deadly, incurable citrus disease putatively caused by the unculturable bacterium, ‘Candidatus Liberibacter asiaticus’ (CLas), and transmitted by Diaphorina citri. Prior studies suggest D. citri transmits CLas in a circulative and propagative manner; however, the precise interactions necessary for CLas transmission remain unknown, and the impact of insect sex on D. citri-CLas interactions is poorly understood despite reports of sex-dependent susceptibilities to CLas. We analyzed the transcriptome, proteome, metabolome, and microbiome of male and female adult D. citri reared on healthy or CLas-infected Citrus medica to determine shared and sex-specific responses of D. citri and its endosymbionts to CLas exposure. More sex-specific than shared D. citri responses to CLas were observed, despite there being no difference between males and females in CLas density or relative abundance. CLas exposure altered the abundance of proteins involved in immunity and cellular and oxidative stress in a sex-dependent manner. CLas exposure impacted cuticular proteins and enzymes involved in chitin degradation, as well as energy metabolism and abundance of the endosymbiont ‘Candidatus Profftella armatura’ in both sexes similarly. Notably, diaphorin, a toxic Profftella-derived metabolite, was more abundant in both sexes with CLas exposure. The responses reported here resulted from a combination of CLas colonization of D. citri as well as the effect of CLas infection on C. medica. Elucidating these impacts on D. citri and their endosymbionts contributes to our understanding of the HLB pathosystem and identifies the responses potentially critical to limiting or promoting CLas acquisition and propagation in both sexes.