Genome organization and interaction with capsid protein in a multipartite RNA virus.
Identifieur interne : 000043 ( Main/Corpus ); précédent : 000042; suivant : 000044Genome organization and interaction with capsid protein in a multipartite RNA virus.
Auteurs : Christian Beren ; Yanxiang Cui ; Antara Chakravarty ; Xue Yang ; A L N. Rao ; Charles M. Knobler ; Z Hong Zhou ; William M. GelbartSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2020.
English descriptors
- KwdEn :
- Bacteriophages (genetics), Bacteriophages (metabolism), Bacteriophages (ultrastructure), Bromovirus (genetics), Bromovirus (metabolism), Bromovirus (ultrastructure), Capsid Proteins (chemistry), Capsid Proteins (genetics), Capsid Proteins (metabolism), Genome, Viral (MeSH), RNA, Viral (genetics), RNA, Viral (metabolism).
- MESH :
- chemical , chemistry : Capsid Proteins.
- genetics : Bacteriophages, Bromovirus, Capsid Proteins, RNA, Viral.
- metabolism : Bacteriophages, Bromovirus, Capsid Proteins, RNA, Viral.
- ultrastructure : Bacteriophages, Bromovirus.
- Genome, Viral.
Abstract
We report the asymmetric reconstruction of the single-stranded RNA (ssRNA) content in one of the three otherwise identical virions of a multipartite RNA virus, brome mosaic virus (BMV). We exploit a sample consisting exclusively of particles with the same RNA content-specifically, RNAs 3 and 4-assembled in planta by agrobacterium-mediated transient expression. We find that the interior of the particle is nearly empty, with most of the RNA genome situated at the capsid shell. However, this density is disordered in the sense that the RNA is not associated with any particular structure but rather, with an ensemble of secondary/tertiary structures that interact with the capsid protein. Our results illustrate a fundamental difference between the ssRNA organization in the multipartite BMV viral capsid and the monopartite bacteriophages MS2 and Qβ for which a dominant RNA conformation is found inside the assembled viral capsids, with RNA density conserved even at the center of the particle. This can be understood in the context of the differing demands on their respective lifecycles: BMV must package separately each of several different RNA molecules and has been shown to replicate and package them in isolated, membrane-bound, cytoplasmic complexes, whereas the bacteriophages exploit sequence-specific "packaging signals" throughout the viral RNA to package their monopartite genomes.
DOI: 10.1073/pnas.1915078117
PubMed: 32358197
PubMed Central: PMC7245085
Links to Exploration step
pubmed:32358197Le document en format XML
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Rao</name><affiliation><nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521; arao@ucr.edu Hong.Zhou@UCLA.edu gelbart@chem.ucla.edu.</nlm:affiliation></affiliation></author><author><name sortKey="Knobler, Charles M" sort="Knobler, Charles M" uniqKey="Knobler C" first="Charles M" last="Knobler">Charles M. Knobler</name><affiliation><nlm:affiliation>Department of Chemistry & Biochemistry, University of California, Los Angeles, CA 90095.</nlm:affiliation></affiliation></author><author><name sortKey="Zhou, Z Hong" sort="Zhou, Z Hong" uniqKey="Zhou Z" first="Z Hong" last="Zhou">Z Hong Zhou</name><affiliation><nlm:affiliation>California NanoSystems Institute, University of California, Los Angeles, CA 90095; arao@ucr.edu Hong.Zhou@UCLA.edu gelbart@chem.ucla.edu.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Microbiology, Immunology & Molecular Genetics, University of California, Los Angeles, CA 90095.</nlm:affiliation></affiliation></author><author><name sortKey="Gelbart, William M" sort="Gelbart, William M" uniqKey="Gelbart W" first="William M" last="Gelbart">William M. Gelbart</name><affiliation><nlm:affiliation>Department of Chemistry & Biochemistry, University of California, Los Angeles, CA 90095; arao@ucr.edu Hong.Zhou@UCLA.edu gelbart@chem.ucla.edu.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>California NanoSystems Institute, University of California, Los Angeles, CA 90095.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Molecular Biology Institute, University of California, Los Angeles, CA 90095.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="eISSN">1091-6490</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Bacteriophages (genetics)</term><term>Bacteriophages (metabolism)</term><term>Bacteriophages (ultrastructure)</term><term>Bromovirus (genetics)</term><term>Bromovirus (metabolism)</term><term>Bromovirus (ultrastructure)</term><term>Capsid Proteins (chemistry)</term><term>Capsid Proteins (genetics)</term><term>Capsid Proteins (metabolism)</term><term>Genome, Viral (MeSH)</term><term>RNA, Viral (genetics)</term><term>RNA, Viral (metabolism)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Capsid Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Bacteriophages</term><term>Bromovirus</term><term>Capsid Proteins</term><term>RNA, Viral</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Bacteriophages</term><term>Bromovirus</term><term>Capsid Proteins</term><term>RNA, Viral</term></keywords><keywords scheme="MESH" qualifier="ultrastructure" xml:lang="en"><term>Bacteriophages</term><term>Bromovirus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Genome, Viral</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">We report the asymmetric reconstruction of the single-stranded RNA (ssRNA) content in one of the three otherwise identical virions of a multipartite RNA virus, brome mosaic virus (BMV). We exploit a sample consisting exclusively of particles with the same RNA content-specifically, RNAs 3 and 4-assembled in planta by agrobacterium-mediated transient expression. We find that the interior of the particle is nearly empty, with most of the RNA genome situated at the capsid shell. However, this density is disordered in the sense that the RNA is not associated with any particular structure but rather, with an ensemble of secondary/tertiary structures that interact with the capsid protein. Our results illustrate a fundamental difference between the ssRNA organization in the multipartite BMV viral capsid and the monopartite bacteriophages MS2 and Qβ for which a dominant RNA conformation is found inside the assembled viral capsids, with RNA density conserved even at the center of the particle. This can be understood in the context of the differing demands on their respective lifecycles: BMV must package separately each of several different RNA molecules and has been shown to replicate and package them in isolated, membrane-bound, cytoplasmic complexes, whereas the bacteriophages exploit sequence-specific "packaging signals" throughout the viral RNA to package their monopartite genomes.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32358197</PMID><DateCompleted><Year>2020</Year><Month>08</Month><Day>10</Day></DateCompleted><DateRevised><Year>2020</Year><Month>11</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN><JournalIssue CitedMedium="Internet"><Volume>117</Volume><Issue>20</Issue><PubDate><Year>2020</Year><Month>05</Month><Day>19</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation></Journal><ArticleTitle>Genome organization and interaction with capsid protein in a multipartite RNA virus.</ArticleTitle><Pagination><MedlinePgn>10673-10680</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1915078117</ELocationID><Abstract><AbstractText>We report the asymmetric reconstruction of the single-stranded RNA (ssRNA) content in one of the three otherwise identical virions of a multipartite RNA virus, brome mosaic virus (BMV). We exploit a sample consisting exclusively of particles with the same RNA content-specifically, RNAs 3 and 4-assembled in planta by agrobacterium-mediated transient expression. We find that the interior of the particle is nearly empty, with most of the RNA genome situated at the capsid shell. However, this density is disordered in the sense that the RNA is not associated with any particular structure but rather, with an ensemble of secondary/tertiary structures that interact with the capsid protein. Our results illustrate a fundamental difference between the ssRNA organization in the multipartite BMV viral capsid and the monopartite bacteriophages MS2 and Qβ for which a dominant RNA conformation is found inside the assembled viral capsids, with RNA density conserved even at the center of the particle. This can be understood in the context of the differing demands on their respective lifecycles: BMV must package separately each of several different RNA molecules and has been shown to replicate and package them in isolated, membrane-bound, cytoplasmic complexes, whereas the bacteriophages exploit sequence-specific "packaging signals" throughout the viral RNA to package their monopartite genomes.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Beren</LastName><ForeName>Christian</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0001-7392-4050</Identifier><AffiliationInfo><Affiliation>Department of Chemistry & Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cui</LastName><ForeName>Yanxiang</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0002-8909-6576</Identifier><AffiliationInfo><Affiliation>California NanoSystems Institute, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chakravarty</LastName><ForeName>Antara</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Xue</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>California NanoSystems Institute, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology, Immunology & Molecular Genetics, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rao</LastName><ForeName>A L N</ForeName><Initials>ALN</Initials><Identifier Source="ORCID">0000-0002-5454-3110</Identifier><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521; arao@ucr.edu Hong.Zhou@UCLA.edu gelbart@chem.ucla.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Knobler</LastName><ForeName>Charles M</ForeName><Initials>CM</Initials><Identifier Source="ORCID">0000-0003-2625-0801</Identifier><AffiliationInfo><Affiliation>Department of Chemistry & Biochemistry, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Z Hong</ForeName><Initials>ZH</Initials><Identifier Source="ORCID">0000-0002-8373-4717</Identifier><AffiliationInfo><Affiliation>California NanoSystems Institute, University of California, Los Angeles, CA 90095; arao@ucr.edu Hong.Zhou@UCLA.edu gelbart@chem.ucla.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology, Immunology & Molecular Genetics, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gelbart</LastName><ForeName>William M</ForeName><Initials>WM</Initials><AffiliationInfo><Affiliation>Department of Chemistry & Biochemistry, University of California, Los Angeles, CA 90095; arao@ucr.edu Hong.Zhou@UCLA.edu gelbart@chem.ucla.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>California NanoSystems Institute, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Molecular Biology Institute, University of California, Los Angeles, CA 90095.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><DataBankList CompleteYN="Y"><DataBank><DataBankName>PDB</DataBankName><AccessionNumberList><AccessionNumber>6VOC</AccessionNumber></AccessionNumberList></DataBank></DataBankList><GrantList CompleteYN="Y"><Grant><GrantID>R01 AI094386</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>05</Month><Day>01</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Proc Natl Acad Sci U S A</MedlineTA><NlmUniqueID>7505876</NlmUniqueID><ISSNLinking>0027-8424</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D036022">Capsid Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C028696">Qbeta ribonucleic acid</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D012367">RNA, Viral</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D001435" MajorTopicYN="N">Bacteriophages</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName><QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017795" MajorTopicYN="N">Bromovirus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName><QualifierName UI="Q000648" MajorTopicYN="N">ultrastructure</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D036022" MajorTopicYN="N">Capsid Proteins</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016679" MajorTopicYN="Y">Genome, Viral</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012367" MajorTopicYN="N">RNA, Viral</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">cryoelectron microscopy</Keyword><Keyword MajorTopicYN="Y">single-stranded RNA</Keyword><Keyword MajorTopicYN="Y">virus</Keyword></KeywordList><CoiStatement>The authors declare no competing interest.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate 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