Paper · 2025 · Frontiers in Plant Science

Bacterial wilt pathogen induced spatial shifts of root-associated microbiome and metabolome of potatoes

Xianjun Lai; Zhouhua He; Shuyan Wang; et al.

13
claims
26
verbatim quotes
10
citations
2
research areas
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Open access · cc-by

Abstract

Introduction Plant root-associated microbiomes play an important role in plant health, yet their responses to bacterial wilt remain unclear poorly understood. Methods This study investigated spatial variations in microbiome and metabolome composition across three root-associated niches—root-surrounding soil, rhizosphere, and endosphere—of healthy and Ralstonia solanacearum -infected potato plants. A total of 36 samples were analyzed, with microbial diversity assessed by full-length 16S rRNA and ITS sequencing, and metabolic profiles characterized using LC-QTOF-MS. Results Alpha diversity analysis revealed that bacterial diversity in healthy plants was consistently higher than in diseased plants, progressively increasing from the root-surrounding soil to the rhizosphere, and most notably in the endosphere, where the Shannon index declined from 5.3 (healthy) to 1.2 (diseased). In contrast, fungal diversity was lower in diseased plants in the root-surrounding soil and rhizosphere, but significantly elevated in the endosphere, suggesting niche-specific microbial responses to pathogen stress. Beta diversity confirmed significant microbiome restructuring under pathogen stress ( R² > 0.5, p = 0.001). Taxonomic analysis showed over 98% dominance of Proteobacteria in the diseased endosphere, where Burkholderia , Pseudomonas , and Massilia enriched in healthy plants were significantly reduced. R. solanacearum infection promotes the enrichment of Fusarium species in both the rhizosphere and endosphere. Metabolomic analysis revealed extensive pathogen-induced metabolic reprogramming, with 299 upregulated and 483 downregulated metabolites in the diseased endosphere, including antimicrobial metabolites such as verruculogen and aurachin A. Network analysis identified XTP as a central metabolite regulating microbial interactions, whereas antimicrobial metabolites exhibited targeted pathogen suppression. O2PLS analysis revealed that pathogen-induced antimicrobial metabolites (e.g., Gentamicin X2, Glutathionylspermine) were associated with Clostridia and Ketobacter in diseased plants, while nucleotide-related compounds (e.g., XTP) correlated with Rhodomicrobium and others, indicating infection-driven microbial adaptation and metabolic restructuring. Discussion These findings provide insights into pathogen-driven disruptions in root microbiomes and suggest potential microbiome engineering strategies for bacterial wilt management.

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Claims 13

Associationobservedoriginal resultpositivemeasured

Claim · model-written summary

Bacterial diversity was higher in healthy than diseased potato plants, especially in the endosphere, where Shannon index fell from 5.3 to 1.2.

Taxon
potatoesSolanum tuberosumt0
Organ / stage
endospheree0
Outcome
bacterial diversitye0
Direction
highere0
Value
5.3 (healthy) to 1.2 (diseased)e0
Comparator
diseased plantse0

Not reportedInteractor

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“bacterial diversity in healthy plants was consistently higher than in diseased plants, progressively increasing from the root-surrounding soil to the rhizosphere, and most notably in the endosphere, where the Shannon index declined from 5.3 (healthy) to 1.2 (diseased)”

✓ located verbatim in the source · abstract, characters 618–886 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Fungal diversity was lower in diseased potato root-surrounding soil and rhizosphere.

Taxon
potatoesSolanum tuberosumt0
Outcome
fungal diversitye0
Direction
lowere0
Comparator
diseased plantse0
Setting
root-surrounding soil and rhizospheree0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“fungal diversity was lower in diseased plants in the root-surrounding soil and rhizosphere”

✓ located verbatim in the source · abstract, characters 901–991 · show in text ↑
Associationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Fungal diversity was significantly elevated in the endosphere of diseased potato plants.

Taxon
potatoesSolanum tuberosumt0
Organ / stage
endospheree0
Outcome
fungal diversitye0
Direction
elevatede0
Comparator
diseased plantse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“fungal diversity was lower in diseased plants in the root-surrounding soil and rhizosphere, but significantly elevated in the endosphere”

✓ located verbatim in the source · abstract, characters 901–1037 · show in text ↑
Associationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Pathogen stress significantly restructured the potato root-associated microbiome.

Taxon
potatoesSolanum tuberosumt0
Treatment
pathogen stresse0
Outcome
microbiome restructuringe0
Value
R² > 0.5e0

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“significant microbiome restructuring under pathogen stress ( R² > 0.5, p = 0.001)”

✓ located verbatim in the source · abstract, characters 1130–1211 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Proteobacteria dominated more than 98% of the diseased potato endosphere.

Taxon
potatoesSolanum tuberosumt0
Organ / stage
diseased endospheree0
Outcome
dominance of Proteobacteriae0
Value
over 98%e0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“over 98% dominance of Proteobacteria in the diseased endosphere”

✓ located verbatim in the source · abstract, characters 1239–1302 · show in text ↑
Associationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Burkholderia, Pseudomonas and Massilia enriched in healthy potato plants were significantly reduced in diseased endosphere.

Taxon
potatoesSolanum tuberosumt0
Outcome
Burkholderia , Pseudomonas , and Massiliae0
Direction
reducede0
Comparator
healthy plantse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“Burkholderia , Pseudomonas , and Massilia enriched in healthy plants were significantly reduced”

✓ located verbatim in the source · abstract, characters 1310–1405 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

R. solanacearum infection enriched Fusarium species in the potato rhizosphere and endosphere.

Taxon
potatoesSolanum tuberosumt0
Organ / stage
rhizosphere and endospheree0
Interactor
R. solanacearumRalstonia solanacearume0pathogen
Outcome
enrichment of Fusarium speciese0
Direction
enrichmente0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗
Ralstonia solanacearum
Ralstonia solanacearum · InteractorClemson University - USDA Cooperative Extension Slide Series, Bugwood.org · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“R. solanacearum infection promotes the enrichment of Fusarium species in both the rhizosphere and endosphere”

✓ located verbatim in the source · abstract, characters 1407–1515 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

In the diseased potato endosphere, 299 metabolites were upregulated.

Taxon
potatoesSolanum tuberosumt0
Organ / stage
diseased endospheree0
Outcome
metabolitese0
Direction
upregulatede0
Value
299e0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“299 upregulated and 483 downregulated metabolites in the diseased endosphere”

✓ located verbatim in the source · abstract, characters 1604–1680 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

In the diseased potato endosphere, 483 metabolites were downregulated.

Taxon
potatoesSolanum tuberosumt0
Organ / stage
diseased endospheree0
Outcome
metabolitese0
Direction
downregulatede0
Value
483e0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“299 upregulated and 483 downregulated metabolites in the diseased endosphere”

✓ located verbatim in the source · abstract, characters 1604–1680 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Network analysis identified XTP as a central metabolite regulating microbial interactions in potatoes.

Taxon
potatoesSolanum tuberosumt0
Compound
XTPe0
Outcome
microbial interactionse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“Network analysis identified XTP as a central metabolite regulating microbial interactions”

✓ located verbatim in the source · abstract, characters 1755–1844 · show in text ↑
Mechanismobservedoriginal resultpositivemeasured

Claim · model-written summary

Antimicrobial metabolites exhibited targeted pathogen suppression in potatoes.

Taxon
potatoesSolanum tuberosumt0
Compound
antimicrobial metabolitese0
Outcome
pathogen suppressione0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“antimicrobial metabolites exhibited targeted pathogen suppression”

✓ located verbatim in the source · abstract, characters 1854–1919 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Gentamicin X2 and Glutathionylspermine were associated with Clostridia and Ketobacter in diseased potato plants.

Taxon
potatoesSolanum tuberosumt0
Compound
Gentamicin X2, Glutathionylsperminee0
Outcome
Clostridia and Ketobactere0
Qualifier
diseased plantse0

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“Gentamicin X2, Glutathionylspermine) were associated with Clostridia and Ketobacter in diseased plants”

✓ located verbatim in the source · abstract, characters 2000–2102 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

XTP correlated with Rhodomicrobium and other microbes in diseased potato plants.

Taxon
potatoesSolanum tuberosumt0
Compound
XTPe0
Outcome
Rhodomicrobium and otherse0

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potatoes”

✓ located verbatim in the source · title, characters 95–103 · show in text ↑
e0

“XTP) correlated with Rhodomicrobium and others”

✓ located verbatim in the source · abstract, characters 2146–2192 · show in text ↑