The Plant Host Can Affect the Encapsidation of Brome Mosaic Virus (BMV) RNA: BMV Virions Are Surprisingly Heterogeneous

Ni, Peng; Vaughan, Robert C.; Tragesser, Brady; Hoover, Haley; Kao, C. Cheng

doi:10.1016/j.jmb.2013.09.007

Cited by 41 publications

(41 citation statements)

References 66 publications

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“…We found that the SGF appears to be dependent on the host species, suggesting the involvement of host factors that differ among host species play a role in its regulation. In agreement with our findings, Ni et al also found that the relative abundances of encapsidated and total RNA segments of BMV were also dependent on the host species 34 . Indeed, when the ratios of the three segments were followed during the progression of infection in two monocot hosts, they converge into stable SGF total (1:2:3 for barley and 1:2:2 for wheat).…”

Section: Discussionsupporting

confidence: 93%

Within-host Evolution of Segments Ratio for the Tripartite Genome ofAlfalfa Mosaic Virus

Wu¹,

Zwart²,

Sánchez‐Navarro³

et al. 2016

Preprint

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The existence of multipartite viruses is an intriguing mystery in evolutionary virology. Several hypotheses suggest benefits that should outweigh the costs of a reduced transmission efficiency and of segregation of coadapted genes associated with encapsidating each segment into a different particle. Advantages range from increasing genome size despite high mutation rates, faster replication, more efficient selection resulting from reassortment during mixed infections, better regulation of gene expression, or enhanced virion stability and cell-to-cell movement. However, support for these hypotheses is scarce. Here we report experiments testing whether an evolutionary stable equilibrium exists for the three genomic RNAs of Alfalfa mosaic virus (AMV). Starting infections with different segment combinations, we found that the relative abundance of each segment evolves towards a constant ratio. Population genetic analyses show that the segment ratio at this equilibrium is determined by frequency-dependent selection. Replication of RNAs 1 and 2 was coupled and collaborative, whereas the replication of RNA 3 interfered with the replication of the other two. We found that the equilibrium solution is slightly different for the total amounts of RNA produced and encapsidated, suggesting that competition exists between all RNAs during encapsidation. Finally, we found that the observed equilibrium appears to be host-species dependent.

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Section: Discussionsupporting

confidence: 93%

Within-host Evolution of Segments Ratio for the Tripartite Genome ofAlfalfa Mosaic Virus

Wu¹,

Zwart²,

Sánchez‐Navarro³

et al. 2016

Preprint

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“…Cryo-EM analysis of the BMV virions suggests that phosphorylation affects capsid-RNA interactions. We used a modified CLIP-seq assay to examine the RNA sequences that contact the BMV capsid as a function of CIP treatment (5,39). The nucleotides in the BMV RNA bound to the capsid were enumerated by determination of the number of sequence reads that contained the nucleotide.…”

Section: Resultsmentioning

confidence: 99%

“…The CP is translated from subgenomic RNA4. In a typical infection, RNA4 is coencapsidated with RNA3 in a 1:1 ratio (4), although the host species can influence the encapsidation of the viral RNAs (5).…”

mentioning

confidence: 99%

Phosphorylation of the Brome Mosaic Virus Capsid Regulates the Timing of Viral Infection

Hoover

Wang

Middleton

et al. 2016

J Virol

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The four brome mosaic virus (BMV) RNAs (RNA1 to RNA4) are encapsidated in three distinct virions that have different disassembly rates in infection. The mechanism for the differential release of BMV RNAs from virions is unknown, since 180 copies of the same coat protein (CP) encapsidate each of the BMV genomic RNAs. Using mass spectrometry, we found that the BMV CP contains a complex pattern of posttranslational modifications. Treatment with phosphatase was found to not significantly affect the stability of the virions containing RNA1 but significantly impacted the stability of the virions that encapsidated BMV RNA2 and RNA3/4. Cryo-electron microscopy reconstruction revealed dramatic structural changes in the capsid and the encapsidated RNA. A phosphomimetic mutation in the flexible N-terminal arm of the CP increased BMV RNA replication and virion produc- T he timing of viral genome release into the infected host cell is critically important to the outcome of infection, as it initiates the race between viral processes and the cellular immune responses against the virus. Even small changes in the timing of viral genome release can result in decreased fitness of the virus (1, 2). The regulation of the release of the viral RNAs is poorly understood, especially for icosahedral viruses.Brome mosaic virus (BMV) is a plant-infecting RNA virus that has served as a model system to study the regulation of RNA virus infection (3). A particularly intriguing feature of BMV is that its tripartite positive-strand RNA genome is encapsidated in three distinct virions. All three virions are required for successful infection. Upon entry into cells, RNA1 and RNA2 direct the translation of the viral replication-associated proteins, while RNA3 encodes the movement protein required for cell-to-cell spread and the coat protein (CP). The CP is translated from subgenomic RNA4. In a typical infection, RNA4 is coencapsidated with RNA3 in a 1:1 ratio (4), although the host species can influence the encapsidation of the viral RNAs (5).The BMV CP has multiple regulatory activities during infection (6, 7). Each BMV capsid contains 180 subunits of the CP arranged in a Tϭ3 symmetry. A CP subunit has structural features similar to those of a histone protein. Both have an intrinsically disordered N-terminal arm rich in positively charged residues followed by sequences that fold into a globular domain (7). The N-terminal arm contributes to the differential encapsidation of BMV RNA, has the ability to translocate from the internal cavity to the outside of the virion, and is preferentially cleaved during proteolysis (8,9). Virions formed by CPs that lack the first 8 residues were found to encapsidate RNA2 well but were labile for the encapsidation of RNA1 (8).The BMV virions can be separated by their density into two populations, one enriched for virions containing RNA1, called B1 virions, and the other enriched for virions that encapsidate RNA2 and RNA3/4, called B2.3/4 virions (9). The B1 virions release RNA1 more rapidly than the B2.3/4 v...

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“…High-throughput DNA sequencing was performed using the Illumina MiSeq system. CLIP-Seq was performed as described previously (17,18). Analyses of MiSeq reads were performed using the Galaxy User Interface.…”

Section: Methodsmentioning

confidence: 99%

“…A protocol that was previously used to examine the interactions between viral proteins with RNA in cells was adapted (17,18) (Fig. 4A).…”

Section: Hnrnp K Can Bind Mir-122 In Cells-mentioning

confidence: 99%

Heterogeneous Ribonucleoprotein K (hnRNP K) Binds miR-122, a Mature Liver-Specific MicroRNA Required for Hepatitis C Virus Replication

Fan

Sutandy

Syu

et al. 2015

Molecular & Cellular Proteomics

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The Plant Host Can Affect the Encapsidation of Brome Mosaic Virus (BMV) RNA: BMV Virions Are Surprisingly Heterogeneous

Cited by 41 publications

References 66 publications

Within-host Evolution of Segments Ratio for the Tripartite Genome ofAlfalfa Mosaic Virus

Within-host Evolution of Segments Ratio for the Tripartite Genome ofAlfalfa Mosaic Virus

Phosphorylation of the Brome Mosaic Virus Capsid Regulates the Timing of Viral Infection

Heterogeneous Ribonucleoprotein K (hnRNP K) Binds miR-122, a Mature Liver-Specific MicroRNA Required for Hepatitis C Virus Replication

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