Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage

The bacterial wilt pathogens in the Ralstonia solanacearum species complex (RSSC) have broad but finite host ranges. Population genetic surveys of RSSC pathogens show that many sequevars (subspecies groups) are predominantly recovered from wilting solanaceous plants. In contrast, strains in the IIB-...

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Main Authors: Jonathan Beutler, Samuel Holden, Stratton Georgoulis, Darrielle Williams, David J. Norman, Tiffany M. Lowe-Power
Format: Article
Language:English
Published: The American Phytopathological Society 2023-09-01
Series:PhytoFrontiers
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/PHYTOFR-06-22-0068-SC
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author Jonathan Beutler
Samuel Holden
Stratton Georgoulis
Darrielle Williams
David J. Norman
Tiffany M. Lowe-Power
author_facet Jonathan Beutler
Samuel Holden
Stratton Georgoulis
Darrielle Williams
David J. Norman
Tiffany M. Lowe-Power
author_sort Jonathan Beutler
collection DOAJ
description The bacterial wilt pathogens in the Ralstonia solanacearum species complex (RSSC) have broad but finite host ranges. Population genetic surveys of RSSC pathogens show that many sequevars (subspecies groups) are predominantly recovered from wilting solanaceous plants. In contrast, strains in the IIB-4 sequevar have been isolated from plants in over a dozen families. Certain IIB-4 lineages have been classified as banana-virulent versus “not pathogenic to banana (NPB).” Prior analysis suggested that the NPB lineage has diverged from the banana-virulent IIB-4 strains. To test this model, we analyzed the phenotypes and phylogeny of a diverse collection of 19 IIB-4 isolates. We used Illumina sequencing to assemble draft genomes of 12 new strains. Based on whole genome phylogenetic analysis, these IIB-4 strains clustered into five subclades. We quantified the virulence of each strain on tomato, banana, melon, and impatiens plants. Overall, the virulence patterns correlated with phylogeny. Banana virulence was restricted to the IIB-4D subclade (N = 4/4 strains) and IIB-4E subclade (N = 1/2 strains). Subclades IIB-4D and IIB-4E are sister subclades, and their closest relative, the IIB-4A-C subclade, lacked virulence on banana. Our data support a revised model in which banana virulence is an innovation within the IIB4D/E subclades. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
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spelling doaj.art-bd197ad945d44ba9a2f4400c72667c962024-02-03T11:51:11ZengThe American Phytopathological SocietyPhytoFrontiers2690-54422023-09-013226226710.1094/PHYTOFR-06-22-0068-SCWhole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 LineageJonathan Beutler0Samuel Holden1Stratton Georgoulis2Darrielle Williams3David J. Norman4Tiffany M. Lowe-Power5Department of Plant Pathology, University of California Davis, Davis, CA 95616, U.S.A.Land and Food Systems, University of British Columbia, Vancouver, BC, CanadaDepartment of Plant Pathology, University of California Davis, Davis, CA 95616, U.S.A.Department of Plant Pathology, University of California Davis, Davis, CA 95616, U.S.A.UF/IFAS Extension, Mid-Florida Research and Education Center, Apopka, FL 32703, U.S.A.Department of Plant Pathology, University of California Davis, Davis, CA 95616, U.S.A.The bacterial wilt pathogens in the Ralstonia solanacearum species complex (RSSC) have broad but finite host ranges. Population genetic surveys of RSSC pathogens show that many sequevars (subspecies groups) are predominantly recovered from wilting solanaceous plants. In contrast, strains in the IIB-4 sequevar have been isolated from plants in over a dozen families. Certain IIB-4 lineages have been classified as banana-virulent versus “not pathogenic to banana (NPB).” Prior analysis suggested that the NPB lineage has diverged from the banana-virulent IIB-4 strains. To test this model, we analyzed the phenotypes and phylogeny of a diverse collection of 19 IIB-4 isolates. We used Illumina sequencing to assemble draft genomes of 12 new strains. Based on whole genome phylogenetic analysis, these IIB-4 strains clustered into five subclades. We quantified the virulence of each strain on tomato, banana, melon, and impatiens plants. Overall, the virulence patterns correlated with phylogeny. Banana virulence was restricted to the IIB-4D subclade (N = 4/4 strains) and IIB-4E subclade (N = 1/2 strains). Subclades IIB-4D and IIB-4E are sister subclades, and their closest relative, the IIB-4A-C subclade, lacked virulence on banana. Our data support a revised model in which banana virulence is an innovation within the IIB4D/E subclades. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/PHYTOFR-06-22-0068-SCbacterial pathogensgenomicshost rangeRalstonia IIB-4Ralstonia solanacearum species complex
spellingShingle Jonathan Beutler
Samuel Holden
Stratton Georgoulis
Darrielle Williams
David J. Norman
Tiffany M. Lowe-Power
Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage
PhytoFrontiers
bacterial pathogens
genomics
host range
Ralstonia IIB-4
Ralstonia solanacearum species complex
title Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage
title_full Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage
title_fullStr Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage
title_full_unstemmed Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage
title_short Whole Genome Sequencing Suggests that “Nonpathogenicity on Banana (NPB)” Is the Ancestral State of the Ralstonia solanacearum IIB-4 Lineage
title_sort whole genome sequencing suggests that nonpathogenicity on banana npb is the ancestral state of the ralstonia solanacearum iib 4 lineage
topic bacterial pathogens
genomics
host range
Ralstonia IIB-4
Ralstonia solanacearum species complex
url https://apsjournals.apsnet.org/doi/10.1094/PHYTOFR-06-22-0068-SC
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