Host plant adaptation drives changes in Diaphorina citri proteome regulation, proteoform expression and transmission of Candidatus Liberibacter asiaticus, the citrus greening pathogen

Authors: Ramsey, John - John; AMMAR, DESOUKY - Retired ARS Employee; MAHONEY, JACLYN - Cornell University; RIVERA, KEITH - Cold Spring Harbor Laboratory; JOHNSON, RICHARD - University Of Washington; IGWE, DAVID - Cornell University; Thannhauser, Theodore - Ted; MACCOSS, MICHAEL - University Of Washington; HALL, DAVID - Retired ARS Employee; Heck, Michelle

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/22/2021
Publication Date: 1/14/2022
Citation: Ramsey, J.S., Ammar, D., Mahoney, J.E., Rivera, K., Johnson, R., Igwe, D.O., Thannhauser, T.W., Maccoss, M.J., Hall, D.G., Heck, M.L. 2022. Host plant adaptation drives changes in Diaphorina citri proteome regulation, proteoform expression and transmission of Candidatus Liberibacter asiaticus, the citrus greening pathogen. Phytopathology. 112:101-115. https://doi.org/10.1094/phyto-06-21-0275-r.
DOI: https://doi.org/10.1094/phyto-06-21-0275-r

Interpretive Summary: Citrus greening disease is the most serious disease of citrus world-wide. The disease is caused by tree infection with a bacterium and that bacterium is spread from tree to tree by a tiny sap-sucking insect vector called the Asian citrus psyllid. In areas where citrus is grown, citrus relatives serve as host plants to the insect vector. ARS scientists in Ithaca, NY and Fort Pierce, Florida, in collaboration with University partners, conducted research to show that movement between host plant species impacts transmission CLas. By analyzing psyllid proteins using proteomics, which is the large scale study of proteins, the team shows that switching host plants causes major changes in the insect's physiology in ways that would be predicted to change several key aspects important to citrus greening transmission. This study further elucidates the complex interactions affecting the ability of the Asian citrus psyllid to spread citrus greening disease and may lead to the development of novel strategies to control the spread of the disease.

Technical Abstract: The Asian citrus psyllid (ACP, Diaphorina citri) is a pest of citrus and the primary insect vector of the bacterial pathogen, ‘Candidatus Liberibacter asiaticus’ (CLas), which is associated with citrus greening disease. The citrus relative Murraya paniculata (orange jasmine) is a host plant of D. citri, but is more resistant to CLas compared to all tested Citrus genotypes. The effect of host switching of D. citri between Citrus medica (citron) and M. paniculata plants on the acquisition and transmission of CLas was investigated. The psyllid CLas titer and the proportion of CLas-infected psyllids decreased in the generations following transfer from CLas-infected citron to healthy M. paniculata plants. Furthermore, after several generations of feeding on M. paniculata, pathogen acquisition (20-40% reduction) and transmission rates (15-20% reduction) in psyllids transferred to CLas-infected citron were reduced compared to psyllids continually maintained on infected citron. Top-down (Difference Gel Electrophoresis) and bottom-up (shotgun MS/MS) proteomics methods were used to identify changes in D. citri protein expression resulting from host plant switching between Citrus macrophylla and M. paniculata. Changes in expression of insect metabolism, immunity, and cytoskeleton proteins were associated with host plant switching. Both transient and sustained feeding on M. paniculata induced distinct patterns of protein expression in D. citri compared to psyllids reared on C. macrophylla. The results point to complex interactions that affect vector competence, and may lead to strategies to control the spread of citrus greening disease.