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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 consist 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

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

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

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

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.[15] 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.[16] 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,[17][18] 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.[19]

Evolutionary origin

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.[20][21] Comparisons have been made between the (-) strand of viroids and the U1 small nuclear ribonucleoprotein particle (snRNPs), implicating that viroids could be escaped introns.[20][21][22][23] Dickson (1981) also observed such homologies within both the (+) and (-) strands of viroids and virusoids.[24] 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.[25]

Virusoids and other circular RNAs are ancient molecules that are being explored with renewed interest.[26][27] 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.[28][29]

Developments

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).[30][31] 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),[32] 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.[32] 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).[33]

References

  1. ^ Symons RH (1991). "The intriguing viroids and virusoids: what is their information content and how did they evolve?" (PDF). Mol. Plant Microbe Interact. 4 (2): 111–21. doi:10.1094/MPMI-4-111. 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 Z, Afzal R. 2013. Life cycle and pathogenesis of hepatitis D virus: a review. World J Hepatol 5: 666–675.
  4. ^ Alves C, Branco C, Cunha C. 2013. Hepatitis δ virus: a peculiar virus. AdvVirol 2013: 560105.
  5. ^ Haseloff, J., Mohamed, N.A. and Symons, R.H. 1982. Nature 299, 316-321.
  6. ^ Randles, J.W., Davies, C., Hatta, T., Gould, A.R., and Francki, R.I.B. 1981. Virology 108, 11 L-122.
  7. ^ Francki, R. I. B. 1985. Plant virus satellites, Ann.Rev.Microbiol.1985.39:151-74
  8. ^ ERIKA LASDA and ROY PARKER. Circular RNAs: diversity of form and function. RNA 20:1829–1842; Published by Cold Spring Harbor Laboratory Press for the RNA Society, 2014.
  9. ^ Roossinck, M. J., Sleat, D., and Palukaitis, P. (1992). Satellite RNAs of plant viruses: structures and biological effects. Microbiol. Rev. 56, 265–279.
  10. ^ Sheldon, C. C. & Symons, R. H. (1993). Is hammerhead self-cleavage involved in the replication of a virusoid in vivo? Virology 194, 463–474.
  11. ^ a b Duncan Gellatly, KayvanMirhadi, SrividhyaVenkataraman and Mounir G. AbouHaidar. Structural and sequence integrity are essential for the replication of the viroid-like satellite RNA of lucerne transient streak virus. Journal of General Virology (2011), 92, 1475–1481.
  12. ^ Rubino, L. & Russo, M. (2010). Properties of a novel satellite RNA associated with tomato bushy stunt virus infections. J Gen Virol 91, 2393–2401.
  13. ^ Francki, R. I. B. (1987). Possible viroid origin: Encapsidated viroid-like RNA.In ‘‘TheViroids’’ (T. O. Diener, Ed.), pp. 205–218. Plenum, New York.
  14. ^ Gast, F.-U., Kempe, D., Spieker, R. L., and Sanger, H. L. (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. J. Mol. Biol. 262, 652–670.
  15. ^ Symons, R. H. (1991). The intriguing viroids and virusoids: What is their information content and how did they evolve? Mol. Plant–Microbe Interact. 4, 111–121.
  16. ^ Song, S. I. & Miller, W. A. (2004). Cis and trans requirements for rolling circle replication of a satellite RNA. J Virol 78, 3072–3082.
  17. ^ Forster, A. C., Davies, C., Sheldon, C. C., Jeffries, A. C., and Symons, R. H. (1988). Self-cleaving viroid and newt RNAs may only be active as dimers. Nature 334, 265–267.
  18. ^ Hernandez, C., Daros, J. A., Elena, S. F., Moya, A., and Flores, R. (1992). The strands of both polarities of a small circular RNA from carnation self-cleavein vitro through alternative double- and single-hammerhead structures. Nucleic Acids Res. 20, 6323–6329.
  19. ^ Diener, T.O.,1981.Areviroidsescapedintrons?Proc.Natl.Acad.Sci.USA78(8), 5014–5015.
  20. ^ a b Dinter Gottlieb. Viroids and virusoids are related to group I introns. Proc. Nati. Acad. Sci. USAVol. 83, pp. 6250-6254, September 1986
  21. ^ a b R.F. Collins, D.L. Gellatly, O.P. Sehgal, M.G. 1998. Abouhaidar. Self-cleaving circular RNA associated with rice yellow mottle virus is the smallest viroid-like RNA. Virology, 241, pp. 269-275
  22. ^ Diener, T.O.,1986.Viroid processing:a model involving the central conserved region and hairpinI.Proc.Natl.Acad.Sci.USA 83(1),58–62.
  23. ^ Diener, T.O.,1989.Circular RNAs:relics of precellular evolution?Proc.Natl.Acad. Sci. USA86(23),9370–9374.
  24. ^ Dickson, E. (1981) Virology 115, 216-221.
  25. ^ 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. doi:10.1007/s002390010203. PMID 11479686. S2CID 779074.
  26. ^ Hsiao KY, Sun HS, Tsai SJ. Circular RNA - New member of noncoding RNA with novel functions.Exp Biol Med (Maywood). 2017 Jun;242(11):1136-1141.
  27. ^ Qu S, Zhong Y, Shang R, Zhang X, Song W, Kjems J, Li H. The emerging landscape of circular RNA in life processes.RNA Biol. 2017 Aug 3;14(8):992-999.
  28. ^ Litholdo CG Jr, da Fonseca GC. Circular RNAs and Plant Stress Responses.Adv Exp Med Biol. 2018;1087:345-353.
  29. ^ Holdt LM, Kohlmaier A, Teupser D. Molecular roles and function of circular RNAs in eukaryotic cells.Cell Mol Life Sci. 2018 Mar;75(6):1071-1098.
  30. ^ Briddon RW, Patil BL, Bagewadi B, Nawaz-ul-Rehman MS, Fauquet CM. Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses.BMCEvol Biol. 2010 Apr 8;10:97. doi: 10.1186/1471-2148-10-97.
  31. ^ AbouHaidar, M.G.,Venkataraman,S.,Golshani,A.,Liu,B.,Ahmad,T.,2014.Novel coding, translation,andgeneexpressionofareplicatingcovalentlyclosed circular RNAof220nt.Proc.Natl.Acad.Sci.USA111(40),14542–14547
  32. ^ a b Lin, N.S., Lee, Y.S., Lin, B.Y., Lee, C.W., Hsu, Y.H., 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. Proc. Natl. Acad. Sci. USA 93, 3138_3142.
  33. ^ Gossele ´, V., Fache ´, I., Meulewaeter, F., Cornelissen, M., Metzlaff, M., 2002.SVISS  A novel transient gene silencing system for gene function discovery and validation in tobacco plants. Plant J. 32, 859-866.
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