The molecular interplay of the establishment of an infection – gene expression of Diaphorina citrigut andCandidatusLiberibacter asiaticus
Authors: de Moura Manoel Bento Flavia , Cecília Darolt Josiane , Laís Merlin Bruna , Penã Leandro , Wulff Nelson Arno , Cônsoli Fernando Luis 
Published: April 2021

CandidatusLiberibacter asiaticus (CLas) is one the causative agents of greening disease in citrus, an unccurable, devastating disease of citrus worldwide. CLas is vectored byDiaphorina citri, and the understanding of the molecular interplay between vector and pathogen will provide additional basis for the development and implementation of successful management strategies. We focused in the molecular interplay occurring in the gut of the vector, a major barrier for CLas invasion and colonization. We investigated the differential expression of vector and CLas genes by analyzing ade novoreference metatranscriptome of the gut of adult psyllids fed of CLas-infected and healthy citrus plants for 1-2, 3-4 and 5-6 days. CLas regulates the immune response of the vector affecting the production of reactive species of oxygen and nitrogen, and the production of antimicrobial peptides. Moreover, CLas overexpressedperoxiredoxinin a protective manner. The major transcript involved in immune expression was related to melanization, aCLIP-domain serine proteasewe believe participates in the wounding of epithelial cells damaged during infection, which is supported by the down-regulation ofpangolin. We also detected that CLas modulates the gut peristalsis of psyllids through the down-regulation oftitin, reducing the elimination of CLas with faeces. The up-regulation of the neuromodulatorarylalkylamine N-acetyltransferaseimplies CLas also interferes with the double brain-gut communication circuitry of the vector. CLas colonizes the gut by expressing twoType IVb pilin flpgenes and several chaperones that can also function as adhesins. We hypothesized biofil formation occurs by the expression of the cold shock protein of CLas. We also describe the interplay during cell invasion and modification, and propose mechanisms CLas uses to invade the host hemocel. We identified several specific targets for the development of strategies directed to interfere with the successful utilization of the psyllid vector by this pathogen.

Author Summary

Huanglongbing (HLB) or greening is an incurable disease causing severe damage to citrus production, making citrus industrial activity unsustainable in several countries around the world. HLB is caused by three species ofCandidatusLiberibacter.Ca.L. asiaticus (CLas), vectored by the psyllidDiaphorina citri, is the prevalent species. Attempts to apply new technologies in the development of strategies for disease and pest management are been made. However, we still miss basic information on this system to efficiently apply the current technologies and envisage the implementation of new approaches for pest control, despite the relevant scientific contribution available. One major gap is regarded to the molecular interplay between CLas and its vector. We focused our attention in the molecular interplay occurring at the first relevant interaction of CLas andD. citri, represented by the gut barrier. We report the transcriptional activity of CLas during the invasion and establishment of the infection in the gut of the vector, as well as the transcriptional activity of the vector in response to the infection. We identified several host genes that are targeted and regulated by CLas as well as several CLas genes that are promising targets for the application of new management strategies.