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Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit

BACKGROUND: Pseudomonas syringae is a widespread bacterial species complex that includes a number of significant plant pathogens. Amongst these, P. syringae pv. actinidiae (Psa) initiated a worldwide pandemic in 2008 on cultivars of Actinidia chinensis var. chinensis. To gain information about the e...

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Autores principales: McAtee, Peter A., Brian, Lara, Curran, Ben, van der Linden, Otto, Nieuwenhuizen, Niels J., Chen, Xiuyin, Henry-Kirk, Rebecca A., Stroud, Erin A., Nardozza, Simona, Jayaraman, Jay, Rikkerink, Erik H. A., Print, Cris G., Allan, Andrew C., Templeton, Matthew D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6238374/
https://www.ncbi.nlm.nih.gov/pubmed/30442113
http://dx.doi.org/10.1186/s12864-018-5197-5
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author McAtee, Peter A.
Brian, Lara
Curran, Ben
van der Linden, Otto
Nieuwenhuizen, Niels J.
Chen, Xiuyin
Henry-Kirk, Rebecca A.
Stroud, Erin A.
Nardozza, Simona
Jayaraman, Jay
Rikkerink, Erik H. A.
Print, Cris G.
Allan, Andrew C.
Templeton, Matthew D.
author_facet McAtee, Peter A.
Brian, Lara
Curran, Ben
van der Linden, Otto
Nieuwenhuizen, Niels J.
Chen, Xiuyin
Henry-Kirk, Rebecca A.
Stroud, Erin A.
Nardozza, Simona
Jayaraman, Jay
Rikkerink, Erik H. A.
Print, Cris G.
Allan, Andrew C.
Templeton, Matthew D.
author_sort McAtee, Peter A.
collection PubMed
description BACKGROUND: Pseudomonas syringae is a widespread bacterial species complex that includes a number of significant plant pathogens. Amongst these, P. syringae pv. actinidiae (Psa) initiated a worldwide pandemic in 2008 on cultivars of Actinidia chinensis var. chinensis. To gain information about the expression of genes involved in pathogenicity we have carried out transcriptome analysis of Psa during the early stages of kiwifruit infection. RESULTS: Gene expression in Psa was investigated during the first five days after infection of kiwifruit plantlets, using RNA-seq. Principal component and heatmap analyses showed distinct phases of gene expression during the time course of infection. The first phase was an immediate transient peak of induction around three hours post inoculation (HPI) that included genes that code for a Type VI Secretion System and nutrient acquisition (particularly phosphate). This was followed by a significant commitment, between 3 and 24 HPI, to the induction of genes encoding the Type III Secretion System (T3SS) and Type III Secreted Effectors (T3SE). Expression of these genes collectively accounted for 6.3% of the bacterial transcriptome at this stage. There was considerable variation in the expression levels of individual T3SEs but all followed the same temporal expression pattern, with the exception of hopAS1, which peaked later in expression at 48 HPI. As infection progressed over the time course of five days, there was an increase in the expression of genes with roles in sugar, amino acid and sulfur transport and the production of alginate and colanic acid. These are both polymers that are major constituents of extracellular polysaccharide substances (EPS) and are involved in biofilm production. Reverse transcription-quantitative PCR (RT-qPCR) on an independent infection time course experiment showed that the expression profile of selected bacterial genes at each infection phase correlated well with the RNA-seq data. CONCLUSIONS: The results from this study indicate that there is a complex remodeling of the transcriptome during the early stages of infection, with at least three distinct phases of coordinated gene expression. These include genes induced during the immediate contact with the host, those involved in the initiation of infection, and finally those responsible for nutrient acquisition. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5197-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-62383742018-11-26 Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit McAtee, Peter A. Brian, Lara Curran, Ben van der Linden, Otto Nieuwenhuizen, Niels J. Chen, Xiuyin Henry-Kirk, Rebecca A. Stroud, Erin A. Nardozza, Simona Jayaraman, Jay Rikkerink, Erik H. A. Print, Cris G. Allan, Andrew C. Templeton, Matthew D. BMC Genomics Research Article BACKGROUND: Pseudomonas syringae is a widespread bacterial species complex that includes a number of significant plant pathogens. Amongst these, P. syringae pv. actinidiae (Psa) initiated a worldwide pandemic in 2008 on cultivars of Actinidia chinensis var. chinensis. To gain information about the expression of genes involved in pathogenicity we have carried out transcriptome analysis of Psa during the early stages of kiwifruit infection. RESULTS: Gene expression in Psa was investigated during the first five days after infection of kiwifruit plantlets, using RNA-seq. Principal component and heatmap analyses showed distinct phases of gene expression during the time course of infection. The first phase was an immediate transient peak of induction around three hours post inoculation (HPI) that included genes that code for a Type VI Secretion System and nutrient acquisition (particularly phosphate). This was followed by a significant commitment, between 3 and 24 HPI, to the induction of genes encoding the Type III Secretion System (T3SS) and Type III Secreted Effectors (T3SE). Expression of these genes collectively accounted for 6.3% of the bacterial transcriptome at this stage. There was considerable variation in the expression levels of individual T3SEs but all followed the same temporal expression pattern, with the exception of hopAS1, which peaked later in expression at 48 HPI. As infection progressed over the time course of five days, there was an increase in the expression of genes with roles in sugar, amino acid and sulfur transport and the production of alginate and colanic acid. These are both polymers that are major constituents of extracellular polysaccharide substances (EPS) and are involved in biofilm production. Reverse transcription-quantitative PCR (RT-qPCR) on an independent infection time course experiment showed that the expression profile of selected bacterial genes at each infection phase correlated well with the RNA-seq data. CONCLUSIONS: The results from this study indicate that there is a complex remodeling of the transcriptome during the early stages of infection, with at least three distinct phases of coordinated gene expression. These include genes induced during the immediate contact with the host, those involved in the initiation of infection, and finally those responsible for nutrient acquisition. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5197-5) contains supplementary material, which is available to authorized users. BioMed Central 2018-11-15 /pmc/articles/PMC6238374/ /pubmed/30442113 http://dx.doi.org/10.1186/s12864-018-5197-5 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
McAtee, Peter A.
Brian, Lara
Curran, Ben
van der Linden, Otto
Nieuwenhuizen, Niels J.
Chen, Xiuyin
Henry-Kirk, Rebecca A.
Stroud, Erin A.
Nardozza, Simona
Jayaraman, Jay
Rikkerink, Erik H. A.
Print, Cris G.
Allan, Andrew C.
Templeton, Matthew D.
Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
title Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
title_full Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
title_fullStr Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
title_full_unstemmed Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
title_short Re-programming of Pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
title_sort re-programming of pseudomonas syringae pv. actinidiae gene expression during early stages of infection of kiwifruit
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6238374/
https://www.ncbi.nlm.nih.gov/pubmed/30442113
http://dx.doi.org/10.1186/s12864-018-5197-5
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