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Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response

The zig-zag model of host-pathogen interaction describes the relative strength of defense response across a spectrum of pathogen-induced plant phenotypes. A stronger defense response results in increased resistance. Here, we investigate the strength of pathogen virulence during disease and place the...

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Autores principales: Wang, Qi, Shakoor, Nadia, Boyher, Adam, Veley, Kira M., Berry, Jeffrey C., Mockler, Todd C., Bart, Rebecca S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7822516/
https://www.ncbi.nlm.nih.gov/pubmed/33428681
http://dx.doi.org/10.1371/journal.ppat.1009175
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author Wang, Qi
Shakoor, Nadia
Boyher, Adam
Veley, Kira M.
Berry, Jeffrey C.
Mockler, Todd C.
Bart, Rebecca S.
author_facet Wang, Qi
Shakoor, Nadia
Boyher, Adam
Veley, Kira M.
Berry, Jeffrey C.
Mockler, Todd C.
Bart, Rebecca S.
author_sort Wang, Qi
collection PubMed
description The zig-zag model of host-pathogen interaction describes the relative strength of defense response across a spectrum of pathogen-induced plant phenotypes. A stronger defense response results in increased resistance. Here, we investigate the strength of pathogen virulence during disease and place these findings in the context of the zig-zag model. Xanthomonas vasicola pv. holcicola (Xvh) causes sorghum bacterial leaf streak. Despite being widespread, this disease has not been described in detail at the molecular level. We divided diverse sorghum genotypes into three groups based on disease symptoms: water-soaked lesions, red lesions, and resistance. Bacterial growth assays confirmed that these three phenotypes represent a range of resistance and susceptibility. To simultaneously reveal defense and virulence responses across the spectrum of disease phenotypes, we performed dual RNA-seq on Xvh-infected sorghum. Consistent with the zig-zag model, the expression of plant defense-related genes was strongest in the resistance interaction. Surprisingly, bacterial virulence genes related to the type III secretion system (T3SS) and type III effectors (T3Es) were also most highly expressed in the resistance interaction. This expression pattern was observed at multiple time points within the sorghum-Xvh pathosystem. Further, a similar expression pattern was observed in Arabidopsis infected with Pseudomonas syringae for effector-triggered immunity via AvrRps4 but not AvrRpt2. Specific metabolites were able to repress the Xvh virulence response in vitro and in planta suggesting a possible signaling mechanism. Taken together, these findings reveal multiple permutations of the continually evolving host-pathogen arms race from the perspective of host defense and pathogen virulence responses.
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spelling pubmed-78225162021-01-29 Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response Wang, Qi Shakoor, Nadia Boyher, Adam Veley, Kira M. Berry, Jeffrey C. Mockler, Todd C. Bart, Rebecca S. PLoS Pathog Research Article The zig-zag model of host-pathogen interaction describes the relative strength of defense response across a spectrum of pathogen-induced plant phenotypes. A stronger defense response results in increased resistance. Here, we investigate the strength of pathogen virulence during disease and place these findings in the context of the zig-zag model. Xanthomonas vasicola pv. holcicola (Xvh) causes sorghum bacterial leaf streak. Despite being widespread, this disease has not been described in detail at the molecular level. We divided diverse sorghum genotypes into three groups based on disease symptoms: water-soaked lesions, red lesions, and resistance. Bacterial growth assays confirmed that these three phenotypes represent a range of resistance and susceptibility. To simultaneously reveal defense and virulence responses across the spectrum of disease phenotypes, we performed dual RNA-seq on Xvh-infected sorghum. Consistent with the zig-zag model, the expression of plant defense-related genes was strongest in the resistance interaction. Surprisingly, bacterial virulence genes related to the type III secretion system (T3SS) and type III effectors (T3Es) were also most highly expressed in the resistance interaction. This expression pattern was observed at multiple time points within the sorghum-Xvh pathosystem. Further, a similar expression pattern was observed in Arabidopsis infected with Pseudomonas syringae for effector-triggered immunity via AvrRps4 but not AvrRpt2. Specific metabolites were able to repress the Xvh virulence response in vitro and in planta suggesting a possible signaling mechanism. Taken together, these findings reveal multiple permutations of the continually evolving host-pathogen arms race from the perspective of host defense and pathogen virulence responses. Public Library of Science 2021-01-11 /pmc/articles/PMC7822516/ /pubmed/33428681 http://dx.doi.org/10.1371/journal.ppat.1009175 Text en © 2021 Wang et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wang, Qi
Shakoor, Nadia
Boyher, Adam
Veley, Kira M.
Berry, Jeffrey C.
Mockler, Todd C.
Bart, Rebecca S.
Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response
title Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response
title_full Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response
title_fullStr Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response
title_full_unstemmed Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response
title_short Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response
title_sort escalation in the host-pathogen arms race: a host resistance response corresponds to a heightened bacterial virulence response
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7822516/
https://www.ncbi.nlm.nih.gov/pubmed/33428681
http://dx.doi.org/10.1371/journal.ppat.1009175
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