Virulence is not directly related to strain success in planta in Clavibacter nebraskensis

ABSTRACT Goss’s wilt and leaf blight of maize is an economically important disease caused by the Gram-positive bacterium, Clavibacter nebraskensis (Cn). Little is known about the ecology and pathogenesis of this bacterium. Here, we used phenotypic assays and a high-throughput whole-genome sequencing...

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Main Authors: Molly Veregge, Cory D. Hirsch, Matthew J. Moscou, Liana Burghardt, Peter Tiffin, Devanshi Khokhani
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:mSystems
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Online Access:https://journals.asm.org/doi/10.1128/msystems.01355-24
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author Molly Veregge
Cory D. Hirsch
Matthew J. Moscou
Liana Burghardt
Peter Tiffin
Devanshi Khokhani
author_facet Molly Veregge
Cory D. Hirsch
Matthew J. Moscou
Liana Burghardt
Peter Tiffin
Devanshi Khokhani
author_sort Molly Veregge
collection DOAJ
description ABSTRACT Goss’s wilt and leaf blight of maize is an economically important disease caused by the Gram-positive bacterium, Clavibacter nebraskensis (Cn). Little is known about the ecology and pathogenesis of this bacterium. Here, we used phenotypic assays and a high-throughput whole-genome sequencing approach to explore among-strain variation in virulence and multistrain reproductive success in planta. Our survey of 41 strains revealed that more recently sampled strains tended to have higher virulence than strains sampled before 2010 and tended to be more genetically divergent from the reference strain, isolated in 1971. More detailed assays with a representative sample of 13 of these strains revealed that host genotype (resistant or susceptible) did not strongly affect strain success and that strain success in planta in multi-strain communities was not closely associated with virulence in single-strain assays. Two weakly virulent strains, CIC354 and CIC370, had the greatest reproductive success, whereas the most highly virulent strains did not significantly change in frequency in any host genotype. A genomic analysis revealed candidate genes, including putative virulence factors (i.e., a secreted cellulase), responsible for among-strain variation in reproductive success.IMPORTANCENon-pathogenic strains of many bacterial pathogens are reported to coexist with pathogenic strains in symptomatic plants. To understand the ecology and pathogenesis of the pathogen population, it is essential to study strain dynamics in the context of the host. We created a community of 13 strains exhibiting diverse virulence phenotypes and used this community to infect the host plant. We compared the strain frequency of these strains before and after the host infection. Contrary to our hypothesis of highly virulent strains being selected by the susceptible host, we found that weakly virulent strains were selected by both resistant and susceptible host lines. We identified several genes associated with strain frequency shifts suggesting their role in strain colonization, virulence, and fitness.
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spelling doaj-art-dbd4b75b18e74d65accd1867be146fc82025-01-21T14:00:28ZengAmerican Society for MicrobiologymSystems2379-50772025-01-0110110.1128/msystems.01355-24Virulence is not directly related to strain success in planta in Clavibacter nebraskensisMolly Veregge0Cory D. Hirsch1Matthew J. Moscou2Liana Burghardt3Peter Tiffin4Devanshi Khokhani5Department of Plant Pathology, University of Minnesota, Twin Cities, Minnesota, USADepartment of Plant Pathology, University of Minnesota, Twin Cities, Minnesota, USADepartment of Plant Pathology, University of Minnesota, Twin Cities, Minnesota, USADepartment of Plant Science, Pennsylvania State University, Center Valley, Pennsylvania, USADepartment of Plant and Microbial Biology, University of Minnesota, Twin Cities, Minnesota, USADepartment of Plant Pathology, University of Minnesota, Twin Cities, Minnesota, USAABSTRACT Goss’s wilt and leaf blight of maize is an economically important disease caused by the Gram-positive bacterium, Clavibacter nebraskensis (Cn). Little is known about the ecology and pathogenesis of this bacterium. Here, we used phenotypic assays and a high-throughput whole-genome sequencing approach to explore among-strain variation in virulence and multistrain reproductive success in planta. Our survey of 41 strains revealed that more recently sampled strains tended to have higher virulence than strains sampled before 2010 and tended to be more genetically divergent from the reference strain, isolated in 1971. More detailed assays with a representative sample of 13 of these strains revealed that host genotype (resistant or susceptible) did not strongly affect strain success and that strain success in planta in multi-strain communities was not closely associated with virulence in single-strain assays. Two weakly virulent strains, CIC354 and CIC370, had the greatest reproductive success, whereas the most highly virulent strains did not significantly change in frequency in any host genotype. A genomic analysis revealed candidate genes, including putative virulence factors (i.e., a secreted cellulase), responsible for among-strain variation in reproductive success.IMPORTANCENon-pathogenic strains of many bacterial pathogens are reported to coexist with pathogenic strains in symptomatic plants. To understand the ecology and pathogenesis of the pathogen population, it is essential to study strain dynamics in the context of the host. We created a community of 13 strains exhibiting diverse virulence phenotypes and used this community to infect the host plant. We compared the strain frequency of these strains before and after the host infection. Contrary to our hypothesis of highly virulent strains being selected by the susceptible host, we found that weakly virulent strains were selected by both resistant and susceptible host lines. We identified several genes associated with strain frequency shifts suggesting their role in strain colonization, virulence, and fitness.https://journals.asm.org/doi/10.1128/msystems.01355-24maizeselect and resequenceClavibacter nebraskensisvirulencestrain fitness
spellingShingle Molly Veregge
Cory D. Hirsch
Matthew J. Moscou
Liana Burghardt
Peter Tiffin
Devanshi Khokhani
Virulence is not directly related to strain success in planta in Clavibacter nebraskensis
mSystems
maize
select and resequence
Clavibacter nebraskensis
virulence
strain fitness
title Virulence is not directly related to strain success in planta in Clavibacter nebraskensis
title_full Virulence is not directly related to strain success in planta in Clavibacter nebraskensis
title_fullStr Virulence is not directly related to strain success in planta in Clavibacter nebraskensis
title_full_unstemmed Virulence is not directly related to strain success in planta in Clavibacter nebraskensis
title_short Virulence is not directly related to strain success in planta in Clavibacter nebraskensis
title_sort virulence is not directly related to strain success in planta in clavibacter nebraskensis
topic maize
select and resequence
Clavibacter nebraskensis
virulence
strain fitness
url https://journals.asm.org/doi/10.1128/msystems.01355-24
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