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The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool

BACKGROUND: Bacterial plant pathogens of the Pectobacterium genus are responsible for a wide spectrum of diseases in plants, including important crops such as potato, tomato, lettuce, and banana. Investigation of the genetic diversity underlying virulence and host specificity can be performed at gen...

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Autores principales: Jonkheer, Eef M., Brankovics, Balázs, Houwers, Ilse M., van der Wolf, Jan M., Bonants, Peter J. M., Vreeburg, Robert A. M., Bollema, Robert, de Haan, Jorn R., Berke, Lidija, Smit, Sandra, de Ridder, Dick, van der Lee, Theo A. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8045196/
https://www.ncbi.nlm.nih.gov/pubmed/33849459
http://dx.doi.org/10.1186/s12864-021-07583-5
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author Jonkheer, Eef M.
Brankovics, Balázs
Houwers, Ilse M.
van der Wolf, Jan M.
Bonants, Peter J. M.
Vreeburg, Robert A. M.
Bollema, Robert
de Haan, Jorn R.
Berke, Lidija
Smit, Sandra
de Ridder, Dick
van der Lee, Theo A. J.
author_facet Jonkheer, Eef M.
Brankovics, Balázs
Houwers, Ilse M.
van der Wolf, Jan M.
Bonants, Peter J. M.
Vreeburg, Robert A. M.
Bollema, Robert
de Haan, Jorn R.
Berke, Lidija
Smit, Sandra
de Ridder, Dick
van der Lee, Theo A. J.
author_sort Jonkheer, Eef M.
collection PubMed
description BACKGROUND: Bacterial plant pathogens of the Pectobacterium genus are responsible for a wide spectrum of diseases in plants, including important crops such as potato, tomato, lettuce, and banana. Investigation of the genetic diversity underlying virulence and host specificity can be performed at genome level by using a comprehensive comparative approach called pangenomics. A pangenomic approach, using newly developed functionalities in PanTools, was applied to analyze the complex phylogeny of the Pectobacterium genus. We specifically used the pangenome to investigate genetic differences between virulent and avirulent strains of P. brasiliense, a potato blackleg causing species dominantly present in Western Europe. RESULTS: Here we generated a multilevel pangenome for Pectobacterium, comprising 197 strains across 19 species, including type strains, with a focus on P. brasiliense. The extensive phylogenetic analysis of the Pectobacterium genus showed robust distinct clades, with most detail provided by 452,388 parsimony-informative single-nucleotide polymorphisms identified in single-copy orthologs. The average Pectobacterium genome consists of 47% core genes, 1% unique genes, and 52% accessory genes. Using the pangenome, we zoomed in on differences between virulent and avirulent P. brasiliense strains and identified 86 genes associated to virulent strains. We found that the organization of genes is highly structured and linked with gene conservation, function, and transcriptional orientation. CONCLUSION: The pangenome analysis demonstrates that evolution in Pectobacteria is a highly dynamic process, including gene acquisitions partly in clusters, genome rearrangements, and loss of genes. Pectobacterium species are typically not characterized by a set of species-specific genes, but instead present themselves using new gene combinations from the shared gene pool. A multilevel pangenomic approach, fusing DNA, protein, biological function, taxonomic group, and phenotypes, facilitates studies in a flexible taxonomic context. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07583-5.
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spelling pubmed-80451962021-04-14 The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool Jonkheer, Eef M. Brankovics, Balázs Houwers, Ilse M. van der Wolf, Jan M. Bonants, Peter J. M. Vreeburg, Robert A. M. Bollema, Robert de Haan, Jorn R. Berke, Lidija Smit, Sandra de Ridder, Dick van der Lee, Theo A. J. BMC Genomics Research Article BACKGROUND: Bacterial plant pathogens of the Pectobacterium genus are responsible for a wide spectrum of diseases in plants, including important crops such as potato, tomato, lettuce, and banana. Investigation of the genetic diversity underlying virulence and host specificity can be performed at genome level by using a comprehensive comparative approach called pangenomics. A pangenomic approach, using newly developed functionalities in PanTools, was applied to analyze the complex phylogeny of the Pectobacterium genus. We specifically used the pangenome to investigate genetic differences between virulent and avirulent strains of P. brasiliense, a potato blackleg causing species dominantly present in Western Europe. RESULTS: Here we generated a multilevel pangenome for Pectobacterium, comprising 197 strains across 19 species, including type strains, with a focus on P. brasiliense. The extensive phylogenetic analysis of the Pectobacterium genus showed robust distinct clades, with most detail provided by 452,388 parsimony-informative single-nucleotide polymorphisms identified in single-copy orthologs. The average Pectobacterium genome consists of 47% core genes, 1% unique genes, and 52% accessory genes. Using the pangenome, we zoomed in on differences between virulent and avirulent P. brasiliense strains and identified 86 genes associated to virulent strains. We found that the organization of genes is highly structured and linked with gene conservation, function, and transcriptional orientation. CONCLUSION: The pangenome analysis demonstrates that evolution in Pectobacteria is a highly dynamic process, including gene acquisitions partly in clusters, genome rearrangements, and loss of genes. Pectobacterium species are typically not characterized by a set of species-specific genes, but instead present themselves using new gene combinations from the shared gene pool. A multilevel pangenomic approach, fusing DNA, protein, biological function, taxonomic group, and phenotypes, facilitates studies in a flexible taxonomic context. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07583-5. BioMed Central 2021-04-14 /pmc/articles/PMC8045196/ /pubmed/33849459 http://dx.doi.org/10.1186/s12864-021-07583-5 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 Article
Jonkheer, Eef M.
Brankovics, Balázs
Houwers, Ilse M.
van der Wolf, Jan M.
Bonants, Peter J. M.
Vreeburg, Robert A. M.
Bollema, Robert
de Haan, Jorn R.
Berke, Lidija
Smit, Sandra
de Ridder, Dick
van der Lee, Theo A. J.
The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
title The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
title_full The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
title_fullStr The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
title_full_unstemmed The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
title_short The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
title_sort pectobacterium pangenome, with a focus on pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8045196/
https://www.ncbi.nlm.nih.gov/pubmed/33849459
http://dx.doi.org/10.1186/s12864-021-07583-5
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