Paper · 2023 · Journal of Virology

A viral protein targets mitochondria and chloroplasts by subverting general import pathways and specific receptors

María Sáiz-Bonilla; Andrea Martín-Merchán; Vicente Pallás; et al.

3
claims
9
verbatim quotes
4
citations
3
research areas
✓
Open access

Abstract

ABSTRACT Dual targeting is a relatively little explored phenomenon by which some proteins are transported to two different subcellular compartments, such as chloroplasts and mitochondria. We previously showed that the R domain and the arm region of the melon necrotic spot virus coat protein could act as a dual-targeting peptide, which shares many relevant features in structure, amino acid composition, and functionality with that of the Thr-tRNA synthetases, the best-studied dual-targeted proteins by far. Here, we show that a viral coat protein hijacks the general pathways for organellar protein import and identifies the coat protein-interacting organellar translocon receptors. Our findings demonstrate for the first time that an exogenous dual-targeted protein uses the general Toc and Tom import systems to reach mitochondria and chloroplasts because it depends on the availability of NbToc75 and NbTom40. Interaction studies, subcellular localization analysis, and viral infection assays in silenced plants revealed the significance of plant receptors, such as the mitochondrion NbOm64 and chloroplast NbToc159A, in this transport. We also show that chloroplast protein translocation impairment could be interlinked with retrograde communication triggering a JA-based response that incidentally impairs viral infection. Future research may profit from our results to better comprehend cellular communication, protein import mechanisms, how preproteins interact with their receptors, and how plant pathogens manipulate host machinery to their ends. IMPORTANCE Many plant proteins and some proteins from plant pathogens are dually targeted to chloroplasts and mitochondria, and are supposed to be transported along the general pathways for organellar protein import, but this issue has not been explored yet. Moreover, organellar translocon receptors exist as families of several members whose functional specialization in different cargos is supposed but not thoroughly studied. This article provides novel insights into such topics showing for the first time that an exogenous protein, the melon necrotic spot virus coat protein, exploits the common Toc/Tom import systems to enter both mitochondria and chloroplasts while identifying the involved specific receptors.

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Claims 3

Mechanismobservedoriginal resultmeasured

Claim · model-written summary

The viral coat protein uses Toc and Tom import systems to reach mitochondria and chloroplasts.

Taxon
plantsViridiplantaee2
Interactor
melon necrotic spot virusMelon necrotic spot viruse1pathogen
Gene
NbToc75 and NbTom40e0
Outcome
reach mitochondria and chloroplastse0

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

Melon necrotic spot virus
Melon necrotic spot virus · InteractorBioSciences BA · CC0 · Wikimedia Commons ↗

Verbatim

e0

“an exogenous dual-targeted protein uses the general Toc and Tom import systems to reach mitochondria and chloroplasts because it depends on the availability of NbToc75 and NbTom40”

✓ located verbatim in the source · abstract, characters 735–914 · show in text ↑
e1

“the melon necrotic spot virus coat protein could act as a dual-targeting peptide”

✓ located verbatim in the source · abstract, characters 249–329 · show in text ↑
e2

“silenced plants”

✓ located verbatim in the source · abstract, characters 1002–1017 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

Plant receptors NbOm64 and NbToc159A are significant for viral coat protein transport.

Taxon
plantsViridiplantaee2
Interactor
melon necrotic spot virusMelon necrotic spot viruse1pathogen
Gene
NbOm64 and chloroplast NbToc159Ae0
Outcome
this transporte0

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

Melon necrotic spot virus
Melon necrotic spot virus · InteractorBioSciences BA · CC0 · Wikimedia Commons ↗

Verbatim

e0

“significance of plant receptors, such as the mitochondrion NbOm64 and chloroplast NbToc159A, in this transport”

✓ located verbatim in the source · abstract, characters 1031–1141 · show in text ↑
e1

“the melon necrotic spot virus coat protein could act as a dual-targeting peptide”

✓ located verbatim in the source · abstract, characters 249–329 · show in text ↑
e2

“silenced plants”

✓ located verbatim in the source · abstract, characters 1002–1017 · show in text ↑
Mechanismauthor interpretationoriginal resultpositivemeasured

Claim · model-written summary

Impaired chloroplast protein translocation may trigger a JA-based response that impairs viral infection.

Taxon
plantsViridiplantaee1
Interactor
melon necrotic spot virusMelon necrotic spot viruse2pathogen
Outcome
viral infectione0
Direction
impairse0
Qualifier
chloroplast protein translocation impairmente0

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

Melon necrotic spot virus
Melon necrotic spot virus · InteractorBioSciences BA · CC0 · Wikimedia Commons ↗

Verbatim

e0

“chloroplast protein translocation impairment could be interlinked with retrograde communication triggering a JA-based response that incidentally impairs viral infection”

✓ located verbatim in the source · abstract, characters 1161–1329 · show in text ↑
e1

“silenced plants”

✓ located verbatim in the source · abstract, characters 1002–1017 · show in text ↑
e2

“the melon necrotic spot virus coat protein, exploits the common Toc/Tom import systems”

✓ located verbatim in the source · abstract, characters 2097–2183 · show in text ↑