Paper · 2024 · PLoS Biology

Umbravirus-like RNA viruses are capable of independent systemic plant infection in the absence of encoded movement proteins

Xiaobao Ying; Sayanta Bera; Jinyuan Liu; et al.

11
claims
19
verbatim quotes
26
citations
2
research areas
✓
Open access · cc-by

Abstract

The signature feature of all plant viruses is the encoding of movement proteins (MPs) that supports the movement of the viral genome into adjacent cells and through the vascular system. The recent discovery of umbravirus-like viruses (ULVs), some of which only encode replication-associated proteins, suggested that they, as with umbraviruses that lack encoded capsid proteins (CPs) and silencing suppressors, would require association with a helper virus to complete an infection cycle. We examined the infection properties of 2 ULVs: citrus yellow vein associated virus 1 (CY1), which only encodes replication proteins, and closely related CY2 from hemp, which encodes an additional protein (ORF5CY2) that was assumed to be an MP. We report that both CY1 and CY2 can independently infect the model plant Nicotiana benthamiana in a phloem-limited fashion when delivered by agroinfiltration. Unlike encoded MPs, ORF5CY2 was dispensable for infection of CY2, but was associated with faster symptom development. Examination of ORF5CY2 revealed features more similar to luteoviruses/poleroviruses/sobemovirus CPs than to 30K class MPs, which all share a similar single jelly-roll domain. In addition, only CY2-infected plants contained virus-like particles (VLPs) associated with CY2 RNA and ORF5CY2. CY1 RNA and a defective (D)-RNA that arises during infection interacted with host protein phloem protein 2 (PP2) in vitro and in vivo, and formed a high molecular weight complex with sap proteins in vitro that was partially resistant to RNase treatment. When CY1 was used as a virus-induced gene silencing (VIGS) vector to target PP2 transcripts, CY1 accumulation was reduced in systemic leaves, supporting the usage of PP2 for systemic movement. ULVs are therefore the first plant viruses encoding replication and CPs but no MPs, and whose systemic movement relies on a host MP. This explains the lack of discernable helper viruses in many ULV-infected plants and evokes comparisons with the initial viruses transferred into plants that must have similarly required host proteins for movement.

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Claims 11

Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

CY1 independently infected Nicotiana benthamiana and remained phloem limited after agroinfiltration.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Treatment
agroinfiltratione0
Interactor
CY1e0pathogen
Outcome
independently infecte0

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

“both CY1 and CY2 can independently infect the model plant Nicotiana benthamiana in a phloem-limited fashion when delivered by agroinfiltration”

✓ located verbatim in the source · abstract, characters 748–890 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

CY2 independently infected Nicotiana benthamiana and remained phloem limited after agroinfiltration.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Treatment
agroinfiltratione0
Interactor
CY2e0pathogen
Outcome
independently infecte0

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

“both CY1 and CY2 can independently infect the model plant Nicotiana benthamiana in a phloem-limited fashion when delivered by agroinfiltration”

✓ located verbatim in the source · abstract, characters 748–890 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

ORF5CY2 was dispensable for CY2 infection.

Taxon
plantt0
Interactor
CY2e0pathogen
Gene
ORF5CY2e0
Outcome
infection of CY2e0

Verbatim

e0

“ORF5CY2 was dispensable for infection of CY2”

✓ located verbatim in the source · abstract, characters 912–956 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Associationobservedoriginal resultnegativemeasured

Claim · model-written summary

ORF5CY2 was associated with faster symptom development.

Taxon
plantt0
Interactor
CY2e0pathogen
Gene
ORF5CY2e0
Outcome
symptom developmente0
Direction
fastere0

Verbatim

e0

“ORF5CY2 was dispensable for infection of CY2, but was associated with faster symptom development”

✓ located verbatim in the source · abstract, characters 912–1008 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

ORF5CY2 features resembled viral capsid proteins more than 30K class movement proteins.

Taxon
plantt0
Gene
ORF5CY2e0
Outcome
features more similar to luteoviruses/poleroviruses/sobemovirus CPs than to 30K class MPse0

Verbatim

e0

“ORF5CY2 revealed features more similar to luteoviruses/poleroviruses/sobemovirus CPs than to 30K class MPs”

✓ located verbatim in the source · abstract, characters 1025–1131 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Virus-like particles associated with CY2 RNA and ORF5CY2 occurred only in CY2-infected plants.

Taxon
plantsViridiplantaee0
Interactor
CY2e0pathogen
Gene
ORF5CY2e0
Outcome
virus-like particles (VLPs) associated with CY2 RNA and ORF5CY2e0

Verbatim

e0

“only CY2-infected plants contained virus-like particles (VLPs) associated with CY2 RNA and ORF5CY2”

✓ located verbatim in the source · abstract, characters 1198–1296 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

CY1 RNA interacted with host PP2 in vitro and in vivo.

Taxon
plantt0
Interactor
CY1e0pathogen
Gene
phloem protein 2 (PP2)e0
Outcome
interacted with host protein phloem protein 2 (PP2)e0

Verbatim

e0

“CY1 RNA and a defective (D)-RNA that arises during infection interacted with host protein phloem protein 2 (PP2) in vitro and in vivo”

✓ located verbatim in the source · abstract, characters 1298–1431 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

A CY1-associated defective RNA interacted with host PP2 in vitro and in vivo.

Taxon
plantt0
Interactor
CY1e0pathogen
Gene
phloem protein 2 (PP2)e0
Outcome
a defective (D)-RNA that arises during infection interacted with host protein phloem protein 2 (PP2)e0

Verbatim

e0

“CY1 RNA and a defective (D)-RNA that arises during infection interacted with host protein phloem protein 2 (PP2) in vitro and in vivo”

✓ located verbatim in the source · abstract, characters 1298–1431 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

CY1 RNA and defective RNA formed an RNase-resistant high molecular weight complex with sap proteins in vitro.

Taxon
plantt0
Interactor
CY1e1pathogen
Outcome
high molecular weight complex with sap proteinse0
Qualifier
partially resistant to RNase treatmente0

Verbatim

e0

“formed a high molecular weight complex with sap proteins in vitro that was partially resistant to RNase treatment”

✓ located verbatim in the source · abstract, characters 1437–1550 · show in text ↑
e1

“CY1 RNA and a defective (D)-RNA”

✓ located verbatim in the source · abstract, characters 1298–1329 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Targeting PP2 transcripts with a CY1 VIGS vector reduced CY1 accumulation in systemic leaves.

Taxon
plantt0
Organ / stage
systemic leavese0
Treatment
virus-induced gene silencing (VIGS) vector to target PP2 transcriptse0
Interactor
CY1e0pathogen
Gene
PP2e0
Outcome
CY1 accumulatione0
Direction
reducede0

Not reportedComparator

Verbatim

e0

“When CY1 was used as a virus-induced gene silencing (VIGS) vector to target PP2 transcripts, CY1 accumulation was reduced in systemic leaves”

✓ located verbatim in the source · abstract, characters 1552–1692 · show in text ↑
t0

“plant infection”

✓ located verbatim in the source · title, characters 64–79 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors infer that ULV systemic movement relies on a host movement protein.

Taxon
plante0
Interactor
ULVse0pathogen
Gene
host MPe0
Outcome
systemic movemente0

Verbatim

e0

“ULVs are therefore the first plant viruses encoding replication and CPs but no MPs, and whose systemic movement relies on a host MP”

✓ located verbatim in the source · abstract, characters 1745–1876 · show in text ↑

loss of function · molecular: metabolites · Nicotiana benthamianaPositive and negative results

35 papers: 10 positive, 25 negative or no effect

24 papers in the same direction as this paper · 10 in the opposite direction

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31 papers more in this group

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Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.