Cross-linking Measurements of the Potato leafroll virus Reveal Protein Interaction Topologies Required for Virion Stability, Aphid Transmission, and Virus–Plant Interactions
Open accessAbstract
Protein interactions are critical determinants of insect transmission for viruses in the family Luteoviridae. Two luteovirid structural proteins, the capsid protein (CP) and the readthrough protein (RTP), contain multiple functional domains that regulate virus transmission. There is no structural information available for these economically important viruses. We used Protein Interaction Reporter (PIR) technology, a strategy that uses chemical cross-linking and high resolution mass spectrometry, to discover topological features of the Potato leafroll virus (PLRV) CP and RTP that are required for the diverse biological functions of PLRV virions. Four cross-linked sites were repeatedly detected, one linking CP monomers, two within the RTP, and one linking the RTP and CP. Virus mutants with triple amino acid deletions immediately adjacent to or encompassing the cross-linked sites were defective in virion stability, RTP incorporation into the capsid, and aphid transmission. Plants infected with a new, infectious PLRV mutant lacking 26 amino acids encompassing a cross-linked site in the RTP exhibited a delay in the appearance of systemic infection symptoms. PIR technology provided the first structural insights into luteoviruses which are crucially lacking and are involved in vector-virus and plant-virus interactions. These are the first cross-linking measurements on any infectious, insect-transmitted virus.
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Chavez et al. utilized a cross-linking strategy, Protein Interaction Reporter technology, to generate cross-links that are cleaved within a mass spectrometer for the identification of interacting protein and peptide sequences.
“Chavez et al. utilized a remarkable cross-linking strategy, Protein Interaction Reporter technology, to generate cross-links that are cleaved within a mass spectrometer for the identification of interacting protein and peptide sequences [99,100].”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [100]
By these means, the authors cross-linked proteins in a purified potato leafroll virus sample and revealed topological interaction data in the virus that are required for virus-plant associations and its transmission across aphid vectors.
“By these means, the authors cross-linked proteins in a purified potato leafroll virus sample and revealed topological interaction data in the virus that are required for virus–plant associations and its transmission across aphid vectors [100].”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [100]
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Self-citation
- Authors
- Chavez, J. D., Cilia, M., Weisbrod, C. R., Ju, H.-J., Eng, J. K., Gray, S. M., & Bruce, J. E.
- Affiliations
- University of Washington (US)
- Agricultural Research Service (US)
- Cornell University (US)
- Corresponding author
- Bruce, James E.
- Venue
- Journal of Proteome Research
- Publisher
- American Chemical Society (ACS)
- Published
- 2012-03-30
- Volume
- 11
- Issue
- 5
- Pages
- 2968-2981
- ISSN
- 1535-3893 (ISSN-L)
- 1535-3907
- PMC
- PMC3402239
- OpenAlex
- W2001828337
- Cited by
- 69
- References
- 76
- Citations by year
- 2026: 4 · 2025: 2 · 2023: 3 · 2022: 2 · 2021: 7 · 2020: 4 · 2019: 7 · 2018: 7 · 2017: 3 · 2016: 6 · 2015: 7 · 2014: 9 · 2013: 6 · 2012: 2
- FWCI
- 8.75
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Proteome Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R01GM086688, R01GM097112)
- National Center for Research Resources (R01RR023334, S10RR025107)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Virus Research Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Phytoplasmas and Hemiptera pathogens
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Keywords
- potato leafroll virus, Luteoviridae, capsid protein, protein-protein interaction, crosslinking, virion stability, aphid transmission, systemic infection, viral mutants, viral structural proteins
- MeSH terms
- Amino Acid Sequence, Animals, Aphids, Binding Sites, Feeding Behavior, Insect Vectors, Molecular Sequence Data, Plant Diseases, Plasmids, Solanum tuberosum, Mass Spectrometry, Nicotiana, Agrobacterium tumefaciens, Virus Assembly, Protein Interaction Mapping, Capsid Proteins, Luteoviridae, Host-Pathogen Interactions
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