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Virusoid

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This article is about the viroid which is dependant on viruses. For the object it is made of, see Viroid. For the object it depends on, see Virus.
Circular satellite RNAs
Virus classification Edit this classification
Informal group: Satellite nucleic acids
Informal group: Circular satellite RNAs

Virusoids are circular single-stranded RNA(s) dependent on viruses for replication and encapsidation.[1] The genome of virusoids consists of several hundred (200–400) nucleotides and does not code for any proteins.

Virusoids are essentially viroids that have been encapsulated by a helper virus coat protein. They are thus similar to viroids in their means of replication (rolling circle replication) and in their lack of genes, but they differ in that viroids do not possess a protein coat. Both virusoids and viroids encode a hammerhead ribozyme.

Virusoids, while being studied in virology, are subviral particles rather than viruses. Since they depend on helper viruses, they are classified as satellites. Virusoids are listed in virological taxonomy as Satellites/Satellite nucleic acids/Subgroup 3: Circular satellite RNA(s).[2]

Definition

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Depending on whether a lax or strict definition is used, the term virusoid may also include Hepatitis D virus (HDV). Like plant virusoids, HDV is circular, single-stranded, and supported by a helper virus (Hepatitis B virus) to form virions; however, the virions possess a much larger genome size (~1700 nt) and encode a protein.[3][4] They also show no sequence similarity with the plant virusoid group.

History

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The first virusoid was discovered in Nicotiana velutina plants infected with Velvet tobacco mottle virus R2 (VTMOV).[5][6] These RNAs have also been referred to as viroid-like RNAs that can infect commercially important agricultural crops and are non–self-replicating single stranded RNAs.[7] RNA replication of virusoids is similar to that of viroids but, unlike viroids, virusoids require specific "helper" viruses.

Replication

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The circular structure of virusoid RNA molecules is ideal for rolling circle replication, in which multiple copies of the genome are generated in an efficient manner from a single replication initiation event.[8] Another advantage to circular RNAs as replication intermediates is that they are inaccessible and resistant to exonucleases. Additionally, their high GC content and high degree of self-complementarity make them very stable against endonucleases. Circular RNAs impose constraints on RNA folding by which secondary structures that are favored for replication differ from those assumed during ribozyme-mediated self-cleavage.

Plant satellite RNAs and virusoids depend on their respective helper viruses for replication, while the helper viruses themselves are dependent upon plants to provide some of the components required for replication.[9] Therefore, a complex interaction involving all three major players including satellites, helper viruses and host plants is essential for satellite / virusoid replication.

A hammerhead ribozyme, not from a virusoid (PDB: 2GOZ​)

satLTSV replication has been shown to occur through the symmetric rolling circle mechanism,[10] wherein the satLTSV self-cleaves both (+) and (-) strands. Both the (+) and (-) strands of satLTSV were found to be equally infectious.[11] Nevertheless, since only the (+) strand is packaged in the LTSV particles, the origin of assembly sequence (OAS) / secondary structure is assumed to be present on the (+) strand only.

Gellatly et al., 2011 demonstrated that the entire satLTSV molecule possesses sequence and structural significance wherein any mutations (insertions / deletions) causing disruption in the overall rod-like structure of the virusoid molecule are lethal to its infectivity.[11] Foreign nucleotides introduced into the molecule will only be tolerated if they preserve the overall cruciform structure of the satLTSV. Furthermore, the introduced foreign sequences are eliminated in successive generations to ultimately reproduce the wild-type satLTSV.

Therefore, in satLTSV RNA, the entire sequence seems to be essential for replication. This contrasts with satRNA of TBSV or the defective-interfering RNAs,[12] in which only a small portion of their respective sequences / secondary structures were found to be sufficient for replication.

Role of ribozyme structures in the self-cleavage and replication of virusoids

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Virusoids structurally resemble the viroids as they possess native secondary structures that form double-stranded rod-like molecules with short terminal branches.[13][14] They also contain hammerhead ribozymes that are involved in autocatalytic cleavage of satRNA multimers during rolling circle replication.[1] It was proposed that the hammerhead ribozyme structure of satLTSV is formed only transiently, similar to that observed by Song & Miller (2004) with satRPV (Cereal yellow dwarf polerovirus serotype RPV) RNA.[15] This hammerhead structure contains a short stem III that is stabilized by only two base-paired nucleotides. This unstable conformation thus suggests that a double hammerhead mode of cleavage takes place. These structures are similar to those reported for CarSV and newt ribozymes,[16][17] which implies an ancient relationship between these divergent RNAs. The observation by Collins et al., 1998 that the dimer of the satRYMV RNA is more efficiently self-cleaved than the monomer is consistent with the double hammerhead mode of cleavage. The self-cleavage of the satRYMV in the (+) strand and not in the (-) strand implies that the satRYMV replicates through an asymmetric mode of rolling circle replication, similar to other sobemoviral satellites with the exception of satLTSV.[18]

Evolutionary origin

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A group I intron (PDB: 1grz​)

Considering properties such as their diminutive size, circular structure and the presence of hammerhead ribozymes, viroids may have had an ancient evolutionary origin distinct from that of the viruses. Likewise, the lack of any sequence similarity between the satellite RNAs and their host viruses, host plants and insect vectors implies that these satellite RNAs have had a spontaneous origin. Alternatively, the siRNAs and microRNAs generated during viral infections may have been amplified by helper virus replicases, whereby these molecules assembled to form satellite RNAs.

Virusoids and viroids have been compared to circular introns due to their size similarity. It has been proposed that virusoids and viroids originated from introns.[19][20] Comparisons have been made between the (-) strand of viroids and the U1 small nuclear ribonucleoprotein particle (snRNPs), implicating that viroids could be escaped introns.[19][20][21][22] Dickson (1981) also observed such homologies within both the (+) and (-) strands of viroids and virusoids.[23] In particular, virusoids and viroids exhibit several structural and sequence homologies to the group I introns such as the self-splicing intron of Tetrahymena thermophila.

A phylogeny based on a manually-adjusted alignment in 2001 suggests that virusoids may form a clade of their own as a sister group to Avsunviroidae, which also possess hammerhead ribozymes. However, the said alignment is not available, making the results hard to reproduce.[24]

Virusoids and other circular RNAs are ancient molecules that are being explored with renewed interest.[25][26] Circular RNAs have been shown to possess a number of functions, ranging from modulation of gene expression, interactions with RNA binding proteins (RBPs) acting as miRNA sponges and have been linked to a number of human diseases, including aging and cancer.[27][28]

Developments

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Abouhaidar et al., 2014 demonstrated the only example of protein translation and messenger RNA activity in the Rice yellow mottle virus small circular satellite RNA (scRYMV).[29][30] This group suggested that the scRYMV be designated as a virusoid satelliteRNA that could serve as a model system for both translation and replication.

The most promising application of these subviral agents is to make specific vectors that can be used for the future development of biological control agents for plant viral diseases. The vector system could be applied for the overexpression and silencing of foreign genes. The unique example of a foreign expression vector is Bamboo mosaic virus satellite RNA (satBaMV),[31] which possesses an open reading frame that encodes a 20-kDa P20 protein. It was observed that when this nonessential ORF region was replaced with a foreign gene, expression of the foreign gene was enhanced or overexpressed.[31] In the case of gene silencing, various satellite RNA-based vectors can be used for sequence-specific inactivation. Satellite Tobacco Mosaic Virus (STMV) was the first subviral agent to be developed as a satellite virus-induced silencing system (SVISS).[32]

References

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  1. ^ a b Symons, Robert H. (1991). "Current Review: The Intriguing Viroids and Virusoids: What Is Their Information Content and How Did They Evolve?". Molecular Plant-Microbe Interactions. 4 (2): 111–121. doi:10.1094/MPMI-4-111. ISSN 0894-0282. PMID 1932808.
  2. ^ "3 - Satellites and Other Virus-dependent Nucleic Acids - Subviral Agents - Subviral Agents (2011)". International Committee on Taxonomy of Viruses (ICTV).
  3. ^ Abbas, Zaigham; Afzal, Rafia (2013). "Life cycle and pathogenesis of hepatitis D virus: A review". World Journal of Hepatology. 5 (12): 666–675. doi:10.4254/wjh.v5.i12.666. ISSN 1948-5182. PMC 3879688. PMID 24409335.
  4. ^ Alves, Carolina; Branco, Cristina; Cunha, Celso (2013). "Hepatitis Delta Virus: A Peculiar Virus". Advances in Virology. 2013: 560105. doi:10.1155/2013/560105. ISSN 1687-8639. PMC 3807834. PMID 24198831.
  5. ^ Haseloff, James; Mohamed, Nizar A.; Symons, Robert H. (September 23, 1982). "Viroid RNAs of cadang-cadang disease of coconuts". Nature. 299 (5881): 316–321. Bibcode:1982Natur.299..316H. doi:10.1038/299316a0. ISSN 1476-4687. S2CID 4232530.
  6. ^ Randles, J.W.; Davies, C.; Hatta, T.; Gould, A.R.; Francki, R.I.B. (January 15, 1981). "Studies on encapsidated viroid-like RNA I. Characterization of velvet tobacco mottle virus". Virology. 108 (1): 111–122. doi:10.1016/0042-6822(81)90531-6. PMID 18635027.
  7. ^ Francki, R. I. B. (October 1985). "Plant Virus Satellites". Annual Review of Microbiology. 39 (1): 151–174. doi:10.1146/annurev.mi.39.100185.001055. ISSN 0066-4227. PMID 3904598.
  8. ^ Lasda, Erika; Parker, Roy (December 2014). "Circular RNAs: diversity of form and function". RNA. 20 (12): 1829–1842. doi:10.1261/rna.047126.114. ISSN 1355-8382. PMC 4238349. PMID 25404635.
  9. ^ Roossinck, M J; Sleat, D; Palukaitis, P (June 1992). "Satellite RNAs of plant viruses: structures and biological effects". Microbiological Reviews. 56 (2): 265–279. doi:10.1128/mr.56.2.265-279.1992. ISSN 0146-0749. PMC 372867. PMID 1620065.
  10. ^ Sheldon, Candice C.; Symons, Robert H. (June 1993). "Is Hammerhead Self-Cleavage Involved in the Replication of a Virusold in Vivo?". Virology. 194 (2): 463–474. doi:10.1006/viro.1993.1285. PMID 7684871.
  11. ^ a b Gellatly, Duncan; Mirhadi, Kayvan; Venkataraman, Srividhya; AbouHaidar, Mounir G. (June 1, 2011). "Structural and sequence integrity are essential for the replication of the viroid-like satellite RNA of lucerne transient streak virus". Journal of General Virology. 92 (6): 1475–1481. doi:10.1099/vir.0.029801-0. ISSN 0022-1317. PMID 21346030.
  12. ^ Rubino, L.; Russo, M. (September 1, 2010). "Properties of a novel satellite RNA associated with tomato bushy stunt virus infections". Journal of General Virology. 91 (9): 2393–2401. doi:10.1099/vir.0.022046-0. ISSN 0022-1317. PMID 20484559.
  13. ^ Francki, R. I. B. (1987). "Possible Viroid Origin". In Diener, T. O. (ed.). The Viroids. Boston, MA: Springer US. pp. 205–218. doi:10.1007/978-1-4613-1855-2_9. ISBN 978-1-4612-9035-3.
  14. ^ Gast, Frank-Ulrich; Kempe, Dirk; Spieker, Reiner Ludwig; Sänger, Heinz Ludwig (October 11, 1996). "Secondary Structure Probing of Potato Spindle Tuber Viroid (PSTVd) and Sequence Comparison with Other Small Pathogenic RNA Replicons Provides Evidence for Central Non-canonical Base-pairs, Large A-rich Loops, and a Terminal Branch". Journal of Molecular Biology. 262 (5): 652–670. doi:10.1006/jmbi.1996.0543. PMID 8876645.
  15. ^ Song, Sang Ik; Miller, W. Allen (March 15, 2004). "cis and trans Requirements for Rolling Circle Replication of a Satellite RNA". Journal of Virology. 78 (6): 3072–3082. doi:10.1128/JVI.78.6.3072-3082.2004. ISSN 0022-538X. PMC 353766. PMID 14990726.
  16. ^ Forster, Anthony C.; Davies, Christopher; Sheldon, Candice C.; Jeffries, Alex C.; Symons, Robert H. (July 1988). "Self-cleaving viroid and newt RNAs may only be active as dimers". Nature. 334 (6179): 265–267. Bibcode:1988Natur.334..265F. doi:10.1038/334265a0. ISSN 0028-0836. PMID 2456468. S2CID 4339403.
  17. ^ Hernández, Carmen; Daròs, José A.; Elena, Santiago F.; Moya, Andrés; Flores, Ricardo (1992). "The strands of both polarities of a small circular RNA from carnation self-cleave in vitro through alternative double- and single-hammerhead structures". Nucleic Acids Research. 20 (23): 6323–6329. doi:10.1093/nar/20.23.6323. ISSN 0305-1048. PMC 334523. PMID 1282239.
  18. ^ Diener, T. O. (August 1981). "Are viroids escaped introns?". Proceedings of the National Academy of Sciences. 78 (8): 5014–5015. Bibcode:1981PNAS...78.5014D. doi:10.1073/pnas.78.8.5014. ISSN 0027-8424. PMC 320322. PMID 16593072.
  19. ^ a b Dinter-Gottlieb, G (September 1986). "Viroids and virusoids are related to group I introns". Proceedings of the National Academy of Sciences. 83 (17): 6250–6254. Bibcode:1986PNAS...83.6250D. doi:10.1073/pnas.83.17.6250. ISSN 0027-8424. PMC 386480. PMID 3462692.
  20. ^ a b Collins, R.F.; Gellatly, D.L.; Sehgal, O.P.; Abouhaidar, M.G. (February 15, 1998). "Self-Cleaving Circular RNA Associated with Rice Yellow Mottle Virus Is the Smallest Viroid-like RNA". Virology. 241 (2): 269–275. doi:10.1006/viro.1997.8962. PMID 9499801.
  21. ^ Diener, T O (January 1986). "Viroid processing: a model involving the central conserved region and hairpin I." Proceedings of the National Academy of Sciences. 83 (1): 58–62. Bibcode:1986PNAS...83...58D. doi:10.1073/pnas.83.1.58. ISSN 0027-8424. PMC 322790. PMID 3455758.
  22. ^ Diener, T O (December 1989). "Circular RNAs: relics of precellular evolution?". Proceedings of the National Academy of Sciences. 86 (23): 9370–9374. Bibcode:1989PNAS...86.9370D. doi:10.1073/pnas.86.23.9370. ISSN 0027-8424. PMC 298497. PMID 2480600.
  23. ^ Dickson, Elizabeth (November 1, 1981). "A model for the involvement of viroids in RNA splicing". Virology. 115 (1): 216–221. doi:10.1016/0042-6822(81)90104-5. ISSN 0042-6822. PMID 7292989.
  24. ^ Elena, Santiago F.; Dopazo, Joaquín; de la Peña, Marcos; Flores, Ricardo; Diener, Theodor O.; Moya, Andrés (August 2001). "Phylogenetic Analysis of Viroid and Viroid-Like Satellite RNAs from Plants: A Reassessment". Journal of Molecular Evolution. 53 (2): 155–159. Bibcode:2001JMolE..53..155E. doi:10.1007/s002390010203. PMID 11479686. S2CID 779074.
  25. ^ Hsiao, Kuei-Yang; Sun, H Sunny; Tsai, Shaw-Jenq (June 2017). "Circular RNA – New member of noncoding RNA with novel functions". Experimental Biology and Medicine. 242 (11): 1136–1141. doi:10.1177/1535370217708978. ISSN 1535-3702. PMC 5478007. PMID 28485684.
  26. ^ Qu, Shibin; Zhong, Yue; Shang, Runze; Zhang, Xuan; Song, Wenjie; Kjems, Jørgen; Li, Haimin (August 3, 2017). "The emerging landscape of circular RNA in life processes". RNA Biology. 14 (8): 992–999. doi:10.1080/15476286.2016.1220473. ISSN 1547-6286. PMC 5680710. PMID 27617908.
  27. ^ Litholdo, Celso Gaspar; da Fonseca, Guilherme Cordenonsi (2018). "Circular RNAs and Plant Stress Responses". In Xiao, Junjie (ed.). Circular RNAs. Advances in Experimental Medicine and Biology. Vol. 1087. Singapore: Springer Singapore. pp. 345–353. doi:10.1007/978-981-13-1426-1_27. ISBN 978-981-13-1425-4. PMID 30259379.
  28. ^ Holdt, Lesca M.; Kohlmaier, Alexander; Teupser, Daniel (March 2018). "Molecular roles and function of circular RNAs in eukaryotic cells". Cellular and Molecular Life Sciences. 75 (6): 1071–1098. doi:10.1007/s00018-017-2688-5. ISSN 1420-682X. PMC 5814467. PMID 29116363.
  29. ^ Briddon, Rob W; Patil, Basavaprabhu L; Bagewadi, Basavaraj; Nawaz-ul-Rehman, Muhammad Shah; Fauquet, Claude M (April 8, 2010). "Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses". BMC Evolutionary Biology. 10 (1): 97. Bibcode:2010BMCEE..10...97B. doi:10.1186/1471-2148-10-97. ISSN 1471-2148. PMC 2858149. PMID 20377896.
  30. ^ AbouHaidar, Mounir Georges; Venkataraman, Srividhya; Golshani, Ashkan; Liu, Bolin; Ahmad, Tauqeer (October 7, 2014). "Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt". Proceedings of the National Academy of Sciences. 111 (40): 14542–14547. Bibcode:2014PNAS..11114542A. doi:10.1073/pnas.1402814111. ISSN 0027-8424. PMC 4209996. PMID 25253891.
  31. ^ a b Lin, N S; Lee, Y S; Lin, B Y; Lee, C W; Hsu, Y H (April 2, 1996). "The open reading frame of bamboo mosaic potexvirus satellite RNA is not essential for its replication and can be replaced with a bacterial gene". Proceedings of the National Academy of Sciences. 93 (7): 3138–3142. Bibcode:1996PNAS...93.3138L. doi:10.1073/pnas.93.7.3138. ISSN 0027-8424. PMC 39775. PMID 8610182.
  32. ^ Gosselé, Véronique; Faché, Ina; Meulewaeter, Frank; Cornelissen, Marc; Metzlaff, Michael (December 2002). "SVISS - a novel transient gene silencing system for gene function discovery and validation in tobacco plants". The Plant Journal. 32 (5): 859–866. doi:10.1046/j.1365-313X.2002.01471.x. PMID 12472699.
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