Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs
We report the biological and structural characterization of umbravirus-like associated RNAs (ulaRNAs), a new category of coat-protein dependent subviral RNA replicons that infect plants. These RNAs encode an RNA-dependent RNA polymerase (RdRp) following a −1 ribosomal frameshift event, are 2.7–4.6 k...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-04-01
|
| Series: | Viruses |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1999-4915/13/4/646 |
| _version_ | 1797538239150555136 |
|---|---|
| author | Jingyuan Liu Elizabeth Carino Sayanta Bera Feng Gao Jared P. May Anne E. Simon |
| author_facet | Jingyuan Liu Elizabeth Carino Sayanta Bera Feng Gao Jared P. May Anne E. Simon |
| author_sort | Jingyuan Liu |
| collection | DOAJ |
| description | We report the biological and structural characterization of umbravirus-like associated RNAs (ulaRNAs), a new category of coat-protein dependent subviral RNA replicons that infect plants. These RNAs encode an RNA-dependent RNA polymerase (RdRp) following a −1 ribosomal frameshift event, are 2.7–4.6 kb in length, and are related to umbraviruses, unlike similar RNA replicons that are related to tombusviruses. Three classes of ulaRNAs are proposed, with citrus yellow vein associated virus (CYVaV) placed in Class 2. With the exception of CYVaV, Class 2 and Class 3 ulaRNAs encode an additional open reading frame (ORF) with movement protein-like motifs made possible by additional sequences just past the RdRp termination codon. The full-length secondary structure of CYVaV was determined using Selective 2’ Hydroxyl Acylation analyzed by Primer Extension (SHAPE) structure probing and phylogenic comparisons, which was used as a template for determining the putative structures of the other Class 2 ulaRNAs, revealing a number of distinctive structural features. The ribosome recoding sites of nearly all ulaRNAs, which differ significantly from those of umbraviruses, may exist in two conformations and are highly efficient. The 3′ regions of Class 2 and Class 3 ulaRNAs have structural elements similar to those of nearly all umbraviruses, and all Class 2 ulaRNAs have a unique, conserved 3′ cap-independent translation enhancer. CYVaV replicates independently in protoplasts, demonstrating that the reported sequence is full-length. Additionally, CYVaV contains a sequence in its 3′ UTR that confers protection to nonsense mediated decay (NMD), thus likely obviating the need for umbravirus ORF3, a known suppressor of NMD. This initial characterization lays down a road map for future investigations into these novel virus-like RNAs. |
| first_indexed | 2024-03-10T12:28:41Z |
| format | Article |
| id | doaj.art-1745b5e0366b44c3b774c42578d76790 |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-10T12:28:41Z |
| publishDate | 2021-04-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-1745b5e0366b44c3b774c42578d767902023-11-21T14:49:27ZengMDPI AGViruses1999-49152021-04-0113464610.3390/v13040646Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAsJingyuan Liu0Elizabeth Carino1Sayanta Bera2Feng Gao3Jared P. May4Anne E. Simon5Department of Cell Biology and Molecular Genetics, University of Maryland College Park, College Park, MD 20742, USADepartment of Cell Biology and Molecular Genetics, University of Maryland College Park, College Park, MD 20742, USADepartment of Cell Biology and Molecular Genetics, University of Maryland College Park, College Park, MD 20742, USASilvec Biologics, Rockville, MD 20850, USADepartment of Cell and Molecular Biology and Biochemistry, University of Missouri-Kansas City, Kansas City, MO 64110, USADepartment of Cell Biology and Molecular Genetics, University of Maryland College Park, College Park, MD 20742, USAWe report the biological and structural characterization of umbravirus-like associated RNAs (ulaRNAs), a new category of coat-protein dependent subviral RNA replicons that infect plants. These RNAs encode an RNA-dependent RNA polymerase (RdRp) following a −1 ribosomal frameshift event, are 2.7–4.6 kb in length, and are related to umbraviruses, unlike similar RNA replicons that are related to tombusviruses. Three classes of ulaRNAs are proposed, with citrus yellow vein associated virus (CYVaV) placed in Class 2. With the exception of CYVaV, Class 2 and Class 3 ulaRNAs encode an additional open reading frame (ORF) with movement protein-like motifs made possible by additional sequences just past the RdRp termination codon. The full-length secondary structure of CYVaV was determined using Selective 2’ Hydroxyl Acylation analyzed by Primer Extension (SHAPE) structure probing and phylogenic comparisons, which was used as a template for determining the putative structures of the other Class 2 ulaRNAs, revealing a number of distinctive structural features. The ribosome recoding sites of nearly all ulaRNAs, which differ significantly from those of umbraviruses, may exist in two conformations and are highly efficient. The 3′ regions of Class 2 and Class 3 ulaRNAs have structural elements similar to those of nearly all umbraviruses, and all Class 2 ulaRNAs have a unique, conserved 3′ cap-independent translation enhancer. CYVaV replicates independently in protoplasts, demonstrating that the reported sequence is full-length. Additionally, CYVaV contains a sequence in its 3′ UTR that confers protection to nonsense mediated decay (NMD), thus likely obviating the need for umbravirus ORF3, a known suppressor of NMD. This initial characterization lays down a road map for future investigations into these novel virus-like RNAs.https://www.mdpi.com/1999-4915/13/4/646umbravirussatellite RNAscoat-dependent RNA repliconnonsense-mediated decaygenome-length RNA structure |
| spellingShingle | Jingyuan Liu Elizabeth Carino Sayanta Bera Feng Gao Jared P. May Anne E. Simon Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs Viruses umbravirus satellite RNAs coat-dependent RNA replicon nonsense-mediated decay genome-length RNA structure |
| title | Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs |
| title_full | Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs |
| title_fullStr | Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs |
| title_full_unstemmed | Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs |
| title_short | Structural Analysis and Whole Genome Mapping of a New Type of Plant Virus Subviral RNA: Umbravirus-Like Associated RNAs |
| title_sort | structural analysis and whole genome mapping of a new type of plant virus subviral rna umbravirus like associated rnas |
| topic | umbravirus satellite RNAs coat-dependent RNA replicon nonsense-mediated decay genome-length RNA structure |
| url | https://www.mdpi.com/1999-4915/13/4/646 |
| work_keys_str_mv | AT jingyuanliu structuralanalysisandwholegenomemappingofanewtypeofplantvirussubviralrnaumbraviruslikeassociatedrnas AT elizabethcarino structuralanalysisandwholegenomemappingofanewtypeofplantvirussubviralrnaumbraviruslikeassociatedrnas AT sayantabera structuralanalysisandwholegenomemappingofanewtypeofplantvirussubviralrnaumbraviruslikeassociatedrnas AT fenggao structuralanalysisandwholegenomemappingofanewtypeofplantvirussubviralrnaumbraviruslikeassociatedrnas AT jaredpmay structuralanalysisandwholegenomemappingofanewtypeofplantvirussubviralrnaumbraviruslikeassociatedrnas AT anneesimon structuralanalysisandwholegenomemappingofanewtypeofplantvirussubviralrnaumbraviruslikeassociatedrnas |