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The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus

BACKGROUND: Candidatus Liberibacter asiaticus (CLas) is one the causative agents of greening disease in citrus, an unccurable, devastating disease of citrus worldwide. CLas is vectored by Diaphorina citri, and the understanding of the molecular interplay between vector and pathogen will provide addi...

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Autores principales: Bento, Flavia Moura Manoel, Darolt, Josiane Cecília, Merlin, Bruna Laís, Penã, Leandro, Wulff, Nelson Arno, Cônsoli, Fernando Luis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8454146/
https://www.ncbi.nlm.nih.gov/pubmed/34544390
http://dx.doi.org/10.1186/s12864-021-07988-2
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author Bento, Flavia Moura Manoel
Darolt, Josiane Cecília
Merlin, Bruna Laís
Penã, Leandro
Wulff, Nelson Arno
Cônsoli, Fernando Luis
author_facet Bento, Flavia Moura Manoel
Darolt, Josiane Cecília
Merlin, Bruna Laís
Penã, Leandro
Wulff, Nelson Arno
Cônsoli, Fernando Luis
author_sort Bento, Flavia Moura Manoel
collection PubMed
description BACKGROUND: Candidatus Liberibacter asiaticus (CLas) is one the causative agents of greening disease in citrus, an unccurable, devastating disease of citrus worldwide. CLas is vectored by Diaphorina 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. RESULTS: We investigated the differential expression of vector and CLas genes by analyzing a de novo reference 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 overexpressed peroxiredoxin, probably in a protective manner. The major transcript involved in immune expression was related to melanization, a CLIP-domain serine protease we believe participates in the wounding of epithelial cells damaged during infection, which is supported by the down-regulation of pangolin. We also detected that CLas modulates the gut peristalsis of psyllids through the down-regulation of titin, reducing the elimination of CLas with faeces. The up-regulation of the neuromodulator arylalkylamine N-acetyltransferase implies CLas also interferes with the double brain-gut communication circuitry of the vector. CLas colonizes the gut by expressing two Type IVb pilin flp genes and several chaperones that can also function as adhesins. We hypothesized biofilm formation occurs by the expression of the cold shock protein of CLas. CONCLUSIONS: The thorough detailed analysis of the transcritome of Ca. L. asiaticus and of D. citri at different time points of their interaction in the gut tissues of the host led to the identification of several host genes targeted for regulation by L. asiaticus, but also bacterial genes coding for potential effector proteins. The identified targets and effector proteins are potential targets for the development of new management strategies directed to interfere with the successful utilization of the psyllid vector by this pathogen. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07988-2.
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spelling pubmed-84541462021-09-21 The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus Bento, Flavia Moura Manoel Darolt, Josiane Cecília Merlin, Bruna Laís Penã, Leandro Wulff, Nelson Arno Cônsoli, Fernando Luis BMC Genomics Research BACKGROUND: Candidatus Liberibacter asiaticus (CLas) is one the causative agents of greening disease in citrus, an unccurable, devastating disease of citrus worldwide. CLas is vectored by Diaphorina 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. RESULTS: We investigated the differential expression of vector and CLas genes by analyzing a de novo reference 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 overexpressed peroxiredoxin, probably in a protective manner. The major transcript involved in immune expression was related to melanization, a CLIP-domain serine protease we believe participates in the wounding of epithelial cells damaged during infection, which is supported by the down-regulation of pangolin. We also detected that CLas modulates the gut peristalsis of psyllids through the down-regulation of titin, reducing the elimination of CLas with faeces. The up-regulation of the neuromodulator arylalkylamine N-acetyltransferase implies CLas also interferes with the double brain-gut communication circuitry of the vector. CLas colonizes the gut by expressing two Type IVb pilin flp genes and several chaperones that can also function as adhesins. We hypothesized biofilm formation occurs by the expression of the cold shock protein of CLas. CONCLUSIONS: The thorough detailed analysis of the transcritome of Ca. L. asiaticus and of D. citri at different time points of their interaction in the gut tissues of the host led to the identification of several host genes targeted for regulation by L. asiaticus, but also bacterial genes coding for potential effector proteins. The identified targets and effector proteins are potential targets for the development of new management strategies directed to interfere with the successful utilization of the psyllid vector by this pathogen. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07988-2. BioMed Central 2021-09-21 /pmc/articles/PMC8454146/ /pubmed/34544390 http://dx.doi.org/10.1186/s12864-021-07988-2 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Bento, Flavia Moura Manoel
Darolt, Josiane Cecília
Merlin, Bruna Laís
Penã, Leandro
Wulff, Nelson Arno
Cônsoli, Fernando Luis
The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus
title The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus
title_full The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus
title_fullStr The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus
title_full_unstemmed The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus
title_short The molecular interplay of the establishment of an infection – gene expression of Diaphorina citri gut and Candidatus Liberibacter asiaticus
title_sort molecular interplay of the establishment of an infection – gene expression of diaphorina citri gut and candidatus liberibacter asiaticus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8454146/
https://www.ncbi.nlm.nih.gov/pubmed/34544390
http://dx.doi.org/10.1186/s12864-021-07988-2
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