Co‐opted cytosolic proteins form condensate substructures within membranous replication organelles of a positive‐strand RNA virus
Summary Positive‐strand RNA viruses co‐opt organellar membranes for biogenesis of viral replication organelles (VROs). Tombusviruses also co‐opt pro‐viral cytosolic proteins to VROs. It is currently not known what type of molecular organization keeps co‐opted proteins sequestered within membranous V...
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| Veröffentlicht in: | The New phytologist 2024-09, Vol.243 (5), p.1917-1935 |
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| container_end_page | 1935 |
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| container_issue | 5 |
| container_start_page | 1917 |
| container_title | The New phytologist |
| container_volume | 243 |
| creator | Lin, Wenwu Nagy, Peter D. |
| description | Summary
Positive‐strand RNA viruses co‐opt organellar membranes for biogenesis of viral replication organelles (VROs). Tombusviruses also co‐opt pro‐viral cytosolic proteins to VROs. It is currently not known what type of molecular organization keeps co‐opted proteins sequestered within membranous VROs.
In this study, we employed tomato bushy stunt virus (TBSV) and carnation Italian ringspot virus (CIRV) – Nicotiana benthamiana pathosystems to identify biomolecular condensate formation in VROs.
We show that TBSV p33 and the CIRV p36 replication proteins sequester glycolytic and fermentation enzymes in unique condensate substructures associated with membranous VROs. We find that p33 and p36 form droplets in vitro driven by intrinsically disordered region. The replication protein organizes partitioning of co‐opted host proteins into droplets. VRO‐associated condensates are critical for local adenosine triphosphate production to support energy for virus replication. We find that co‐opted endoplasmic reticulum membranes and actin filaments form meshworks within and around VRO condensates, contributing to unique composition and structure. We propose that p33/p36 organize liquid–liquid phase separation of co‐opted concentrated host proteins in condensate substructures within membranous VROs.
Overall, we demonstrate that subverted membranes and condensate substructures co‐exist and are critical for VRO functions. The replication proteins induce and connect the two substructures within VROs.
See also the Commentary on this article by May, 243: 1636–1638. |
| doi_str_mv | 10.1111/nph.19691 |
| format | Article |
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Positive‐strand RNA viruses co‐opt organellar membranes for biogenesis of viral replication organelles (VROs). Tombusviruses also co‐opt pro‐viral cytosolic proteins to VROs. It is currently not known what type of molecular organization keeps co‐opted proteins sequestered within membranous VROs.
In this study, we employed tomato bushy stunt virus (TBSV) and carnation Italian ringspot virus (CIRV) – Nicotiana benthamiana pathosystems to identify biomolecular condensate formation in VROs.
We show that TBSV p33 and the CIRV p36 replication proteins sequester glycolytic and fermentation enzymes in unique condensate substructures associated with membranous VROs. We find that p33 and p36 form droplets in vitro driven by intrinsically disordered region. The replication protein organizes partitioning of co‐opted host proteins into droplets. VRO‐associated condensates are critical for local adenosine triphosphate production to support energy for virus replication. We find that co‐opted endoplasmic reticulum membranes and actin filaments form meshworks within and around VRO condensates, contributing to unique composition and structure. We propose that p33/p36 organize liquid–liquid phase separation of co‐opted concentrated host proteins in condensate substructures within membranous VROs.
Overall, we demonstrate that subverted membranes and condensate substructures co‐exist and are critical for VRO functions. The replication proteins induce and connect the two substructures within VROs.
See also the Commentary on this article by May, 243: 1636–1638.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19691</identifier><identifier>PMID: 38515267</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Actin ; Actin Cytoskeleton - metabolism ; Adenosine triphosphate ; ATP ; Biogenesis ; biomolecular condensate ; Biomolecular Condensates - metabolism ; Bushy stunt ; Carmovirus - metabolism ; Carmovirus - physiology ; Condensates ; Cytosol - metabolism ; Cytosol - virology ; Droplets ; Endoplasmic reticulum ; Endoplasmic Reticulum - metabolism ; Fermentation ; Filaments ; Glycolysis ; Intracellular Membranes - metabolism ; Intracellular Membranes - virology ; Liquid phases ; Membranes ; Nicotiana - virology ; Organelles ; Organelles - metabolism ; Organelles - virology ; Phase separation ; plant RNA virus ; Plant viruses ; Proteins ; Replication ; RNA viruses ; Tomatoes ; Tombusvirus - physiology ; Viral Proteins - metabolism ; Viral replication ; Virus Replication ; Viruses ; virus–host interaction</subject><ispartof>The New phytologist, 2024-09, Vol.243 (5), p.1917-1935</ispartof><rights>2024 The Author(s). © 2024 New Phytologist Foundation.</rights><rights>2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3531-94d2bb086ef34c1311a06a641c0483db20ff27de1146ed1ce4239d364ed00b3b3</citedby><cites>FETCH-LOGICAL-c3531-94d2bb086ef34c1311a06a641c0483db20ff27de1146ed1ce4239d364ed00b3b3</cites><orcidid>0000-0003-4164-1237</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.19691$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19691$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,27929,27930,45579,45580</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38515267$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lin, Wenwu</creatorcontrib><creatorcontrib>Nagy, Peter D.</creatorcontrib><title>Co‐opted cytosolic proteins form condensate substructures within membranous replication organelles of a positive‐strand RNA virus</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Positive‐strand RNA viruses co‐opt organellar membranes for biogenesis of viral replication organelles (VROs). Tombusviruses also co‐opt pro‐viral cytosolic proteins to VROs. It is currently not known what type of molecular organization keeps co‐opted proteins sequestered within membranous VROs.
In this study, we employed tomato bushy stunt virus (TBSV) and carnation Italian ringspot virus (CIRV) – Nicotiana benthamiana pathosystems to identify biomolecular condensate formation in VROs.
We show that TBSV p33 and the CIRV p36 replication proteins sequester glycolytic and fermentation enzymes in unique condensate substructures associated with membranous VROs. We find that p33 and p36 form droplets in vitro driven by intrinsically disordered region. The replication protein organizes partitioning of co‐opted host proteins into droplets. VRO‐associated condensates are critical for local adenosine triphosphate production to support energy for virus replication. We find that co‐opted endoplasmic reticulum membranes and actin filaments form meshworks within and around VRO condensates, contributing to unique composition and structure. We propose that p33/p36 organize liquid–liquid phase separation of co‐opted concentrated host proteins in condensate substructures within membranous VROs.
Overall, we demonstrate that subverted membranes and condensate substructures co‐exist and are critical for VRO functions. The replication proteins induce and connect the two substructures within VROs.
See also the Commentary on this article by May, 243: 1636–1638.</description><subject>Actin</subject><subject>Actin Cytoskeleton - metabolism</subject><subject>Adenosine triphosphate</subject><subject>ATP</subject><subject>Biogenesis</subject><subject>biomolecular condensate</subject><subject>Biomolecular Condensates - metabolism</subject><subject>Bushy stunt</subject><subject>Carmovirus - metabolism</subject><subject>Carmovirus - physiology</subject><subject>Condensates</subject><subject>Cytosol - metabolism</subject><subject>Cytosol - virology</subject><subject>Droplets</subject><subject>Endoplasmic reticulum</subject><subject>Endoplasmic Reticulum - metabolism</subject><subject>Fermentation</subject><subject>Filaments</subject><subject>Glycolysis</subject><subject>Intracellular Membranes - metabolism</subject><subject>Intracellular Membranes - virology</subject><subject>Liquid phases</subject><subject>Membranes</subject><subject>Nicotiana - virology</subject><subject>Organelles</subject><subject>Organelles - metabolism</subject><subject>Organelles - virology</subject><subject>Phase separation</subject><subject>plant RNA virus</subject><subject>Plant viruses</subject><subject>Proteins</subject><subject>Replication</subject><subject>RNA viruses</subject><subject>Tomatoes</subject><subject>Tombusvirus - physiology</subject><subject>Viral Proteins - metabolism</subject><subject>Viral replication</subject><subject>Virus Replication</subject><subject>Viruses</subject><subject>virus–host interaction</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kcFOHSEUhomp0VvrwhdoSLppF6MwMNxhaW5aNTHWmDbpjjBwpmJmYARGc3fduO8z9klEr-3CpGzO5js_H_wIHVBySMs58tP1IZVC0i20oFzIqqVs-QYtCKnbSnDxYxe9TemGECIbUe-gXdY2tKnFcoEeVuHPr99hymCxWeeQwuAMnmLI4HzCfYgjNsFb8ElnwGnuUo6zyXOEhO9dvnYejzB2UfswJxxhKvs6u-BxiD-1h2EoYOixxlNILrs7KPeVDO0tvro4xncuzukd2u71kGD_Ze6h718-f1udVudfT85Wx-eVYQ2jleS27jrSCugZN5RRqonQglNDeMtsV5O-r5cWaPkEsNQAr5m0THCwhHSsY3vo4ya3PPB2hpTV6JIpjkW06KtaLjkhtJGioB9eoTdhjr7YKVYMeCMZfaI-bSgTQ0oRejVFN-q4VpSop25U6UY9d1PY9y-JczeC_Uf-LaMARxvg3g2w_n-Surg83UQ-AlLsnTI</recordid><startdate>202409</startdate><enddate>202409</enddate><creator>Lin, Wenwu</creator><creator>Nagy, Peter D.</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-4164-1237</orcidid></search><sort><creationdate>202409</creationdate><title>Co‐opted cytosolic proteins form condensate substructures within membranous replication organelles of a positive‐strand RNA virus</title><author>Lin, Wenwu ; Nagy, Peter D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3531-94d2bb086ef34c1311a06a641c0483db20ff27de1146ed1ce4239d364ed00b3b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Actin</topic><topic>Actin Cytoskeleton - metabolism</topic><topic>Adenosine triphosphate</topic><topic>ATP</topic><topic>Biogenesis</topic><topic>biomolecular condensate</topic><topic>Biomolecular Condensates - metabolism</topic><topic>Bushy stunt</topic><topic>Carmovirus - metabolism</topic><topic>Carmovirus - physiology</topic><topic>Condensates</topic><topic>Cytosol - metabolism</topic><topic>Cytosol - virology</topic><topic>Droplets</topic><topic>Endoplasmic reticulum</topic><topic>Endoplasmic Reticulum - metabolism</topic><topic>Fermentation</topic><topic>Filaments</topic><topic>Glycolysis</topic><topic>Intracellular Membranes - metabolism</topic><topic>Intracellular Membranes - virology</topic><topic>Liquid phases</topic><topic>Membranes</topic><topic>Nicotiana - virology</topic><topic>Organelles</topic><topic>Organelles - metabolism</topic><topic>Organelles - virology</topic><topic>Phase separation</topic><topic>plant RNA virus</topic><topic>Plant viruses</topic><topic>Proteins</topic><topic>Replication</topic><topic>RNA viruses</topic><topic>Tomatoes</topic><topic>Tombusvirus - physiology</topic><topic>Viral Proteins - metabolism</topic><topic>Viral replication</topic><topic>Virus Replication</topic><topic>Viruses</topic><topic>virus–host interaction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lin, Wenwu</creatorcontrib><creatorcontrib>Nagy, Peter D.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lin, Wenwu</au><au>Nagy, Peter D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Co‐opted cytosolic proteins form condensate substructures within membranous replication organelles of a positive‐strand RNA virus</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2024-09</date><risdate>2024</risdate><volume>243</volume><issue>5</issue><spage>1917</spage><epage>1935</epage><pages>1917-1935</pages><issn>0028-646X</issn><issn>1469-8137</issn><eissn>1469-8137</eissn><abstract>Summary
Positive‐strand RNA viruses co‐opt organellar membranes for biogenesis of viral replication organelles (VROs). Tombusviruses also co‐opt pro‐viral cytosolic proteins to VROs. It is currently not known what type of molecular organization keeps co‐opted proteins sequestered within membranous VROs.
In this study, we employed tomato bushy stunt virus (TBSV) and carnation Italian ringspot virus (CIRV) – Nicotiana benthamiana pathosystems to identify biomolecular condensate formation in VROs.
We show that TBSV p33 and the CIRV p36 replication proteins sequester glycolytic and fermentation enzymes in unique condensate substructures associated with membranous VROs. We find that p33 and p36 form droplets in vitro driven by intrinsically disordered region. The replication protein organizes partitioning of co‐opted host proteins into droplets. VRO‐associated condensates are critical for local adenosine triphosphate production to support energy for virus replication. We find that co‐opted endoplasmic reticulum membranes and actin filaments form meshworks within and around VRO condensates, contributing to unique composition and structure. We propose that p33/p36 organize liquid–liquid phase separation of co‐opted concentrated host proteins in condensate substructures within membranous VROs.
Overall, we demonstrate that subverted membranes and condensate substructures co‐exist and are critical for VRO functions. The replication proteins induce and connect the two substructures within VROs.
See also the Commentary on this article by May, 243: 1636–1638.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>38515267</pmid><doi>10.1111/nph.19691</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0003-4164-1237</orcidid></addata></record> |
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| subjects | Actin Actin Cytoskeleton - metabolism Adenosine triphosphate ATP Biogenesis biomolecular condensate Biomolecular Condensates - metabolism Bushy stunt Carmovirus - metabolism Carmovirus - physiology Condensates Cytosol - metabolism Cytosol - virology Droplets Endoplasmic reticulum Endoplasmic Reticulum - metabolism Fermentation Filaments Glycolysis Intracellular Membranes - metabolism Intracellular Membranes - virology Liquid phases Membranes Nicotiana - virology Organelles Organelles - metabolism Organelles - virology Phase separation plant RNA virus Plant viruses Proteins Replication RNA viruses Tomatoes Tombusvirus - physiology Viral Proteins - metabolism Viral replication Virus Replication Viruses virus–host interaction |
| title | Co‐opted cytosolic proteins form condensate substructures within membranous replication organelles of a positive‐strand RNA virus |
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