Paper · 2026 · PLoS Pathogens

Natural genetic variation of a single amino acid in beet necrotic yellow vein virus P31 protein modulates evasion of plant ubiquitination-mediated antiviral immunity

Zhi-Hong Guo; Xin-Yu Qin; Meng-Ke Zhou; et al.

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claims
15
verbatim quotes
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citations
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Open access · cc-by

Abstract

Plant virus evolution frequently leads to the emergence of highly virulent strains, posing persistent threats to global crop production. However, the mechanisms by which viral evolution enables evasion of plant defense responses remain poorly understood. Here, we found that Benyvirus necrobetae (beet necrotic yellow vein virus, BNYVV), causing the most destructive rhizomania disease in sugar beet worldwide, exhibits distinct pathogenicity associated with different virus isolates. Two Chinese isolates from Inner Mongolia (NM) and Xin Jiang (XJ) exhibit significantly higher virulence than the Japanese isolate O11 and Germany isolate OW1. Moreover, the high pathogenicity is attributed to the Arg-147 residue in P31NM and P31XJ. The P31 proteins of these isolates exhibit enhanced protein stability, compared with P31O11 and P31OW1 carrying a Lys-147 residue. Furthermore, the E3 ubiquitin ligase Hmg-CoA reductase degradation 1 (HRD1) targets the P31O11 Lys-147 for ubiquitination and subsequent degradation. Whereas, the P31NM Arg-147 evades HRD1-mediated degradation, conferring a virulence advantage. Overexpression of HRD1 obviously inhibits BNYVVO11 infection, rather than BNYVVNM. Moreover, knockout of NbHRD1 in Nicotiana benthamiana enhanced susceptibility to BNYVV infection. Collectively, our findings demonstrate an ongoing evolutionary arms race, in which HRD1 is a critical antiviral component by ubiquitinating viral proteins, while natural mutations in viral genomes enable evasion of host defense.

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Claims 8

Observationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

NM and XJ viral isolates had significantly higher virulence than O11 and OW1.

Outcome
virulencee0
Direction
highere0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Two Chinese isolates from Inner Mongolia (NM) and Xin Jiang (XJ) exhibit significantly higher virulence than the Japanese isolate O11 and Germany isolate OW1.”

✓ located verbatim in the source · abstract, characters 485–643 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

High viral pathogenicity was attributed to Arg-147 in P31NM and P31XJ.

Gene
Arg-147 residue in P31NM and P31XJe0
Outcome
high pathogenicitye0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“the high pathogenicity is attributed to the Arg-147 residue in P31NM and P31XJ.”

✓ located verbatim in the source · abstract, characters 654–733 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

P31 proteins with Arg-147 had enhanced stability relative to Lys-147 variants.

Gene
P31 proteinse0
Outcome
protein stabilitye0
Direction
enhancede0
Comparator
P31O11 and P31OW1e0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“The P31 proteins of these isolates exhibit enhanced protein stability, compared with P31O11 and P31OW1 carrying a Lys-147 residue.”

✓ located verbatim in the source · abstract, characters 734–864 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

HRD1 targets P31O11 Lys-147 for ubiquitination and degradation.

Gene
HRD1e0
Outcome
ubiquitination and subsequent degradatione0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“the E3 ubiquitin ligase Hmg-CoA reductase degradation 1 (HRD1) targets the P31O11 Lys-147 for ubiquitination and subsequent degradation.”

✓ located verbatim in the source · abstract, characters 878–1014 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

P31NM Arg-147 evaded HRD1 degradation, gaining a virulence advantage.

Gene
P31NM Arg-147e0
Outcome
virulence advantagee0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“the P31NM Arg-147 evades HRD1-mediated degradation, conferring a virulence advantage.”

✓ located verbatim in the source · abstract, characters 1024–1109 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

HRD1 overexpression inhibited BNYVVO11 infection.

Treatment
Overexpression of HRD1e0
Outcome
BNYVVO11 infectione0
Direction
inhibitse0
Comparator
BNYVVNMe0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Overexpression of HRD1 obviously inhibits BNYVVO11 infection, rather than BNYVVNM.”

✓ located verbatim in the source · abstract, characters 1110–1192 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

HRD1 overexpression did not inhibit BNYVVNM infection.

Treatment
Overexpression of HRD1e0
Outcome
BNYVVNMe0
Direction
rather thane0
Comparator
BNYVVO11e0

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

Beta vulgaris
Beta vulgaris · TaxonMichael Bakker Paiva · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Overexpression of HRD1 obviously inhibits BNYVVO11 infection, rather than BNYVVNM.”

✓ located verbatim in the source · abstract, characters 1110–1192 · show in text ↑
t0

“beet”

✓ located verbatim in the source · title, characters 52–56 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

NbHRD1 knockout increased Nicotiana benthamiana susceptibility to BNYVV.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Treatment
knockout of NbHRD1e0
Outcome
susceptibility to BNYVV infectione0
Direction
enhancede0

Not reportedComparator

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

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“knockout of NbHRD1 in Nicotiana benthamiana enhanced susceptibility to BNYVV infection.”

✓ located verbatim in the source · abstract, characters 1203–1290 · show in text ↑