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== Definition ==
== 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.<ref name=:17>Abbas Z, Afzal R. 2013. Life cycle and pathogenesis of hepatitis D virus: a review. World J Hepatol 5: 666–675.</ref><ref name=:18>Alves C, Branco C, Cunha C. 2013. Hepatitis δ virus: a peculiar virus. AdvVirol 2013: 560105.</ref> They also show no sequence similarity with the plant virusoid group.
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.<ref>{{Cite journal |last=Abbas |first=Zaigham |last2=Afzal |first2=Rafia |date=2013 |title=Life cycle and pathogenesis of hepatitis D virus: A review |url=http://www.wjgnet.com/1948-5182/full/v5/i12/666.htm |journal=World Journal of Hepatology |language=en |volume=5 |issue=12 |pages=666–675 |doi=10.4254/wjh.v5.i12.666 |issn=1948-5182 |pmc=PMC3879688 |pmid=24409335}}</ref><ref>{{Cite journal |last=Alves |first=Carolina |last2=Branco |first2=Cristina |last3=Cunha |first3=Celso |date=2013 |title=Hepatitis Delta Virus: A Peculiar Virus |url=http://www.hindawi.com/journals/av/2013/560105/ |journal=Advances in Virology |language=en |volume=2013 |pages=1–11 |doi=10.1155/2013/560105 |issn=1687-8639 |pmc=PMC3807834 |pmid=24198831}}</ref> They also show no sequence similarity with the plant virusoid group.


==History==
==History==


The first virusoid was discovered in ''[[Nicotiana velutina]]'' plants infected with Velvet tobacco mottle virus R2 (VTMOV).<ref name=:2>Haseloff, J., Mohamed, N.A. and Symons, R.H. 1982. Nature 299, 316-321.</ref><ref name=:3>Randles, J.W., Davies, C., Hatta, T., Gould, A.R., and Francki, R.I.B. 1981. Virology 108, 11 L-122.</ref> 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.<ref name=:4>Francki, R. I. B. 1985. Plant virus satellites, Ann.Rev.Microbiol.1985.39:151-74</ref> RNA replication of virusoids is similar to that of viroids but, unlike viroids, virusoids require specific "helper" viruses.
The first virusoid was discovered in ''[[Nicotiana velutina]]'' plants infected with Velvet tobacco mottle virus R2 (VTMOV).<ref>{{Cite journal |last=Haseloff |first=James |last2=Mohamed |first2=Nizar A. |last3=Symons |first3=Robert H. |date=September 23, 1982 |title=Viroid RNAs of cadang-cadang disease of coconuts |url=https://www.nature.com/articles/299316a0 |journal=Nature |language=en |volume=299 |issue=5881 |pages=316–321 |doi=10.1038/299316a0 |issn=1476-4687}}</ref><ref name=":3">{{Cite journal |last=Randles |first=J.W. |last2=Davies |first2=C. |last3=Hatta |first3=T. |last4=Gould |first4=A.R. |last5=Francki |first5=R.I.B. |date=January 15, 1981 |title=Studies on encapsidated viroid-like RNA I. Characterization of velvet tobacco mottle virus |url=https://linkinghub.elsevier.com/retrieve/pii/0042682281905316 |journal=Virology |language=en |volume=108 |issue=1 |pages=111–122 |doi=10.1016/0042-6822(81)90531-6}}</ref> 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.<ref name=":4">{{Cite journal |last=Francki |first=R. I. B. |date=October 1985 |title=PLANT VIRUS SATELLITES |url=https://www.annualreviews.org/doi/10.1146/annurev.mi.39.100185.001055 |journal=Annual Review of Microbiology |language=en |volume=39 |issue=1 |pages=151–174 |doi=10.1146/annurev.mi.39.100185.001055 |issn=0066-4227}}</ref> RNA replication of virusoids is similar to that of viroids but, unlike viroids, virusoids require specific "helper" viruses.


==Replication==
==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.<ref name=:5>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.</ref> Another advantage to circular RNAs as replication intermediates is that they are inaccessible and resistant to [[Exonuclease|exonucleases.]] Additionally, their high GC content and high degree of self-complementarity make them very stable against [[endonuclease]]s. 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.
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.<ref name=":5">{{Cite journal |last=Lasda |first=Erika |last2=Parker |first2=Roy |date=December 2014 |title=Circular RNAs: diversity of form and function |url=http://rnajournal.cshlp.org/lookup/doi/10.1261/rna.047126.114 |journal=RNA |language=en |volume=20 |issue=12 |pages=1829–1842 |doi=10.1261/rna.047126.114 |issn=1355-8382 |pmc=PMC4238349 |pmid=25404635}}</ref> Another advantage to circular RNAs as replication intermediates is that they are inaccessible and resistant to [[Exonuclease|exonucleases.]] Additionally, their high GC content and high degree of self-complementarity make them very stable against [[endonuclease]]s. 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.<ref name=:6>Roossinck, M. J., Sleat, D., and Palukaitis, P. (1992). Satellite RNAs of plant viruses: structures and biological effects. ''Microbiol. Rev''. 56, 265–279.</ref> Therefore, a complex interaction involving all three major players including satellites, helper viruses and host plants is essential for satellite / virusoid replication.  
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.<ref name=":6">{{Cite journal |last=Roossinck |first=M J |last2=Sleat |first2=D |last3=Palukaitis |first3=P |date=June 1992 |title=Satellite RNAs of plant viruses: structures and biological effects |url=https://journals.asm.org/doi/10.1128/mr.56.2.265-279.1992 |journal=Microbiological Reviews |language=en |volume=56 |issue=2 |pages=265–279 |doi=10.1128/mr.56.2.265-279.1992 |issn=0146-0749 |pmc=PMC372867 |pmid=1620065}}</ref> Therefore, a complex interaction involving all three major players including satellites, helper viruses and host plants is essential for satellite / virusoid replication.  


[[File:Hammerhead ribozyme ribbons.png|thumb|A hammerhead ribozyme, not from a virusoid ({{PDB|2GOZ}})]]
[[File:Hammerhead ribozyme ribbons.png|thumb|A hammerhead ribozyme, not from a virusoid ({{PDB|2GOZ}})]]
satLTSV replication has been shown to occur through the symmetric rolling circle mechanism,<ref name=:7>Sheldon, C. C. & Symons, R. H. (1993). Is hammerhead self-cleavage involved in the replication of a virusoid in vivo? Virology 194, 463–474.</ref> wherein the satLTSV self-cleaves both (+) and (-) strands. Both the (+) and (-) strands of satLTSV were found to be equally infectious.<ref name=:8>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.</ref> 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.
satLTSV replication has been shown to occur through the symmetric rolling circle mechanism,<ref name=":7">{{Cite journal |last=Sheldon |first=Candice C. |last2=Symons |first2=Robert H. |date=June 1993 |title=Is Hammerhead Self-Cleavage Involved in the Replication of a Virusold in Vivo? |url=https://linkinghub.elsevier.com/retrieve/pii/S0042682283712857 |journal=Virology |language=en |volume=194 |issue=2 |pages=463–474 |doi=10.1006/viro.1993.1285}}</ref> wherein the satLTSV self-cleaves both (+) and (-) strands. Both the (+) and (-) strands of satLTSV were found to be equally infectious.<ref name=":8">{{Cite journal |last=Gellatly |first=Duncan |last2=Mirhadi |first2=Kayvan |last3=Venkataraman |first3=Srividhya |last4=AbouHaidar |first4=Mounir G. |date=June 1, 2011 |title=Structural and sequence integrity are essential for the replication of the viroid-like satellite RNA of lucerne transient streak virus |url=https://www.microbiologyresearch.org/content/journal/jgv/10.1099/vir.0.029801-0 |journal=Journal of General Virology |language=en |volume=92 |issue=6 |pages=1475–1481 |doi=10.1099/vir.0.029801-0 |issn=0022-1317}}</ref> 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.<ref name=:8/> 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.
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.<ref name=:8/> 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,<ref name=:9>Rubino, L. & Russo, M. (2010). Properties of a novel satellite RNA associated with tomato bushy stunt virus infections. J Gen Virol 91, 2393–2401.</ref> in which only a small portion of their respective sequences / secondary structures were found to be sufficient for replication.   
Therefore, in satLTSV RNA, the entire sequence seems to be essential for replication. This contrasts with satRNA of TBSV or the defective-interfering RNAs,<ref name=":9">{{Cite journal |last=Rubino |first=L. |last2=Russo |first2=M. |date=September 1, 2010 |title=Properties of a novel satellite RNA associated with tomato bushy stunt virus infections |url=https://www.microbiologyresearch.org/content/journal/jgv/10.1099/vir.0.022046-0 |journal=Journal of General Virology |language=en |volume=91 |issue=9 |pages=2393–2401 |doi=10.1099/vir.0.022046-0 |issn=0022-1317}}</ref> 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==
==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.<ref name=:10>Francki, R. I. B. (1987). Possible viroid origin: Encapsidated viroid-like RNA.''In'' ‘‘TheViroids’’ (T. O. Diener, Ed.), pp. 205–218. Plenum, New York.</ref><ref name=:11>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.</ref> They also contain hammerhead ribozymes that are involved in autocatalytic cleavage of satRNA multimers during rolling circle replication.<ref name=:12>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.</ref> 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.<ref name=:13>Song, S. I. & Miller, W. A. (2004). Cis and trans requirements for rolling circle replication of a satellite RNA. J Virol 78, 3072–3082.</ref> 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,<ref name=:14>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.</ref><ref name=:15>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-cleave''in vitro'' through alternative double- and single-hammerhead structures. ''Nucleic Acids Res.'' 20, 6323–6329.</ref> 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.<ref name=:16>Diener, T.O.,1981.Areviroidsescapedintrons?Proc.Natl.Acad.Sci.USA78(8), 5014–5015.</ref>
Virusoids structurally resemble the viroids as they possess native secondary structures that form double-stranded rod-like molecules with short terminal branches.<ref name=":10">{{Cite book |last=Francki |first=R. I. B. |title=Possible Viroid Origin |date=1987 |url=http://link.springer.com/10.1007/978-1-4613-1855-2_9 |work=The Viroids |pages=205–218 |editor-last=Diener |editor-first=T. O. |place=Boston, MA |publisher=Springer US |language=en |doi=10.1007/978-1-4613-1855-2_9 |isbn=978-1-4612-9035-3}}</ref><ref name=":11">{{Cite journal |last=Gast |first=Frank-Ulrich |last2=Kempe |first2=Dirk |last3=Spieker |first3=Reiner Ludwig |last4=Sänger |first4=Heinz Ludwig |date=October 11, 1996 |title=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 |url=https://linkinghub.elsevier.com/retrieve/pii/S0022283696905434 |journal=Journal of Molecular Biology |language=en |volume=262 |issue=5 |pages=652–670 |doi=10.1006/jmbi.1996.0543}}</ref> They also contain hammerhead ribozymes that are involved in autocatalytic cleavage of satRNA multimers during rolling circle replication.<ref name=":12">{{Cite journal |last=Symons |first=Robert H. |date=1991 |title=Current Review The Intriguing Viroids and Virusoids: What Is Their Information Content and How Did They Evolve? |url=http://www.apsnet.org/publications/mpmi/backissues/Documents/1991Abstracts/Microbe04-111.htm |journal=Molecular Plant-Microbe Interactions |volume=4 |issue=2 |pages=111 |doi=10.1094/MPMI-4-111 |issn=0894-0282}}</ref> 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.<ref name=":13">{{Cite journal |last=Song |first=Sang Ik |last2=Miller |first2=W. Allen |date=March 15, 2004 |title=cis and trans Requirements for Rolling Circle Replication of a Satellite RNA |url=https://journals.asm.org/doi/10.1128/JVI.78.6.3072-3082.2004 |journal=Journal of Virology |language=en |volume=78 |issue=6 |pages=3072–3082 |doi=10.1128/JVI.78.6.3072-3082.2004 |issn=0022-538X |pmc=PMC353766 |pmid=14990726}}</ref> 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,<ref name=":14">{{Cite journal |last=Forster |first=Anthony C. |last2=Davies |first2=Christopher |last3=Sheldon |first3=Candice C. |last4=Jeffries |first4=Alex C. |last5=Symons |first5=Robert H. |date=July 1988 |title=Self-cleaving viroid and newt RNAs may only be active as dimers |url=http://www.nature.com/articles/334265a0 |journal=Nature |language=en |volume=334 |issue=6179 |pages=265–267 |doi=10.1038/334265a0 |issn=0028-0836}}</ref><ref name=":15">{{Cite journal |last=Hernández |first=Carmen |last2=Daròs |first2=José A. |last3=Elena |first3=Santiago F. |last4=Moya |first4=Andrés |last5=Flores |first5=Ricardo |date=1992 |title=The strands of both polarities of a small circular RNA from carnation self-cleave in vitro through alternative double- and single-hammerhead structures |url=https://academic.oup.com/nar/article-lookup/doi/10.1093/nar/20.23.6323 |journal=Nucleic Acids Research |language=en |volume=20 |issue=23 |pages=6323–6329 |doi=10.1093/nar/20.23.6323 |issn=0305-1048 |pmc=PMC334523 |pmid=1282239}}</ref> 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.<ref name=":16">{{Cite journal |last=Diener |first=T. O. |date=August 1981 |title=Are viroids escaped introns? |url=https://pnas.org/doi/full/10.1073/pnas.78.8.5014 |journal=Proceedings of the National Academy of Sciences |language=en |volume=78 |issue=8 |pages=5014–5015 |doi=10.1073/pnas.78.8.5014 |issn=0027-8424 |pmc=PMC320322 |pmid=16593072}}</ref>


==Evolutionary origin==
==Evolutionary origin==
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Considering properties such as their diminutive size, circular structure and the presence of [[hammerhead ribozyme]]s, 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.
Considering properties such as their diminutive size, circular structure and the presence of [[hammerhead ribozyme]]s, 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.<ref name=:19>Dinter Gottlieb. Viroids and virusoids are related to group I introns. Proc. Nati. Acad. Sci. USAVol. 83, pp. 6250-6254, September 1986</ref><ref name=:20>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</ref> Comparisons have been made between the (-) strand of viroids and the U1 small nuclear ribonucleoprotein particle ([[snRNP]]s), implicating that viroids could be escaped introns.<ref name=:19/><ref name=:20/><ref name=:21>Diener, T.O.,1986.Viroid processing:a model involving the central conserved region and hairpinI.Proc.Natl.Acad.Sci.USA 83(1),58–62.</ref><ref name=:22>Diener, T.O.,1989.Circular RNAs:relics of precellular evolution?Proc.Natl.Acad. Sci. USA86(23),9370–9374.</ref> Dickson (1981) also observed such homologies within both the (+) and (-) strands of viroids and virusoids.<ref name=:23>Dickson, E. (1981) Virology 115, 216-221.</ref> 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]]''.
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.<ref name=":19">{{Cite journal |last=Dinter-Gottlieb |first=G |date=September 1986 |title=Viroids and virusoids are related to group I introns. |url=https://pnas.org/doi/full/10.1073/pnas.83.17.6250 |journal=Proceedings of the National Academy of Sciences |language=en |volume=83 |issue=17 |pages=6250–6254 |doi=10.1073/pnas.83.17.6250 |issn=0027-8424 |pmc=PMC386480 |pmid=3462692}}</ref><ref name=":20">{{Cite journal |last=Collins |first=R.F. |last2=Gellatly |first2=D.L. |last3=Sehgal |first3=O.P. |last4=Abouhaidar |first4=M.G. |date=February 15, 1998 |title=Self-Cleaving Circular RNA Associated with Rice Yellow Mottle Virus Is the Smallest Viroid-like RNA |url=https://linkinghub.elsevier.com/retrieve/pii/S0042682297989625 |journal=Virology |language=en |volume=241 |issue=2 |pages=269–275 |doi=10.1006/viro.1997.8962}}</ref> Comparisons have been made between the (-) strand of viroids and the U1 small nuclear ribonucleoprotein particle ([[snRNP]]s), implicating that viroids could be escaped introns.<ref name=:19/><ref name=:20/><ref name=":21">{{Cite journal |last=Diener |first=T O |date=January 1986 |title=Viroid processing: a model involving the central conserved region and hairpin I. |url=https://pnas.org/doi/full/10.1073/pnas.83.1.58 |journal=Proceedings of the National Academy of Sciences |language=en |volume=83 |issue=1 |pages=58–62 |doi=10.1073/pnas.83.1.58 |issn=0027-8424 |pmc=PMC322790 |pmid=3455758}}</ref><ref name=":22">{{Cite journal |last=Diener |first=T O |date=December 1989 |title=Circular RNAs: relics of precellular evolution? |url=https://pnas.org/doi/full/10.1073/pnas.86.23.9370 |journal=Proceedings of the National Academy of Sciences |language=en |volume=86 |issue=23 |pages=9370–9374 |doi=10.1073/pnas.86.23.9370 |issn=0027-8424 |pmc=PMC298497 |pmid=2480600}}</ref> Dickson (1981) also observed such homologies within both the (+) and (-) strands of viroids and virusoids.<ref name=":23">{{Cite journal |last=Dickson |first=Elizabeth |date=November 1, 1981 |title=A model for the involvement of viroids in RNA splicing |url=https://www.sciencedirect.com/science/article/pii/0042682281901045 |journal=Virology |language=en |volume=115 |issue=1 |pages=216–221 |doi=10.1016/0042-6822(81)90104-5 |issn=0042-6822}}</ref> 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 [[Reproducibility|hard to reproduce]].<ref>{{cite journal |last1=Elena |first1=Santiago F. |last2=Dopazo |first2=Joaquín |last3=de la Peña |first3=Marcos |last4=Flores |first4=Ricardo |last5=Diener |first5=Theodor O. |last6=Moya |first6=Andrés |title=Phylogenetic Analysis of Viroid and Viroid-Like Satellite RNAs from Plants: A Reassessment |journal=Journal of Molecular Evolution |date=August 2001 |volume=53 |issue=2 |pages=155–159 |doi=10.1007/s002390010203|pmid=11479686 |bibcode=2001JMolE..53..155E |s2cid=779074 }}</ref>
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 [[Reproducibility|hard to reproduce]].<ref>{{cite journal |last1=Elena |first1=Santiago F. |last2=Dopazo |first2=Joaquín |last3=de la Peña |first3=Marcos |last4=Flores |first4=Ricardo |last5=Diener |first5=Theodor O. |last6=Moya |first6=Andrés |title=Phylogenetic Analysis of Viroid and Viroid-Like Satellite RNAs from Plants: A Reassessment |journal=Journal of Molecular Evolution |date=August 2001 |volume=53 |issue=2 |pages=155–159 |doi=10.1007/s002390010203|pmid=11479686 |bibcode=2001JMolE..53..155E |s2cid=779074 }}</ref>


Virusoids and other circular RNAs are ancient molecules that are being explored with renewed interest.<ref name=:24>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.</ref><ref name=:25>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.</ref> 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.<ref name=:26>Litholdo CG Jr, da Fonseca GC. Circular RNAs and Plant Stress Responses.Adv Exp Med Biol. 2018;1087:345-353.</ref><ref name=:27>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.</ref>
Virusoids and other circular RNAs are ancient molecules that are being explored with renewed interest.<ref name=":24">{{Cite journal |last=Hsiao |first=Kuei-Yang |last2=Sun |first2=H Sunny |last3=Tsai |first3=Shaw-Jenq |date=June 2017 |title=Circular RNA – New member of noncoding RNA with novel functions |url=http://journals.sagepub.com/doi/10.1177/1535370217708978 |journal=Experimental Biology and Medicine |language=en |volume=242 |issue=11 |pages=1136–1141 |doi=10.1177/1535370217708978 |issn=1535-3702 |pmc=PMC5478007 |pmid=28485684}}</ref><ref name=":25">{{Cite journal |last=Qu |first=Shibin |last2=Zhong |first2=Yue |last3=Shang |first3=Runze |last4=Zhang |first4=Xuan |last5=Song |first5=Wenjie |last6=Kjems |first6=Jørgen |last7=Li |first7=Haimin |date=August 3, 2017 |title=The emerging landscape of circular RNA in life processes |url=https://www.tandfonline.com/doi/full/10.1080/15476286.2016.1220473 |journal=RNA Biology |language=en |volume=14 |issue=8 |pages=992–999 |doi=10.1080/15476286.2016.1220473 |issn=1547-6286 |pmc=PMC5680710 |pmid=27617908}}</ref> 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.<ref name=":26">{{Cite book |last=Litholdo |first=Celso Gaspar |title=Circular RNAs |last2=da Fonseca |first2=Guilherme Cordenonsi |date=2018 |work= |publisher=Springer Singapore |isbn=978-981-13-1425-4 |editor-last=Xiao |editor-first=Junjie |volume=1087 |place=Singapore |pages=345–353 |language=en |chapter=Circular RNAs and Plant Stress Responses |doi=10.1007/978-981-13-1426-1_27 |chapter-url=http://link.springer.com/10.1007/978-981-13-1426-1_27}}</ref><ref name=":27">{{Cite journal |last=Holdt |first=Lesca M. |last2=Kohlmaier |first2=Alexander |last3=Teupser |first3=Daniel |date=March 2018 |title=Molecular roles and function of circular RNAs in eukaryotic cells |url=http://link.springer.com/10.1007/s00018-017-2688-5 |journal=Cellular and Molecular Life Sciences |language=en |volume=75 |issue=6 |pages=1071–1098 |doi=10.1007/s00018-017-2688-5 |issn=1420-682X |pmc=PMC5814467 |pmid=29116363}}</ref>


==Developments==
==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).<ref name=:28>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.</ref><ref name=:29>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</ref> This group suggested that the scRYMV be designated as a virusoid satelliteRNA that could serve as a model system for both translation and replication.
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).<ref name=":28">{{Cite journal |last=Briddon |first=Rob W |last2=Patil |first2=Basavaprabhu L |last3=Bagewadi |first3=Basavaraj |last4=Nawaz-ul-Rehman |first4=Muhammad Shah |last5=Fauquet |first5=Claude M |date=April 8, 2010 |title=Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses |url=https://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-10-97 |journal=BMC Evolutionary Biology |language=en |volume=10 |issue=1 |pages=97 |doi=10.1186/1471-2148-10-97 |issn=1471-2148 |pmc=PMC2858149 |pmid=20377896}}</ref><ref name=":29">{{Cite journal |last=AbouHaidar |first=Mounir Georges |last2=Venkataraman |first2=Srividhya |last3=Golshani |first3=Ashkan |last4=Liu |first4=Bolin |last5=Ahmad |first5=Tauqeer |date=October 7, 2014 |title=Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt |url=https://pnas.org/doi/full/10.1073/pnas.1402814111 |journal=Proceedings of the National Academy of Sciences |language=en |volume=111 |issue=40 |pages=14542–14547 |doi=10.1073/pnas.1402814111 |issn=0027-8424 |pmc=PMC4209996 |pmid=25253891}}</ref> 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 cis-regulatory element|Bamboo mosaic virus satellite RNA]] (satBaMV),<ref name=:30>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.</ref> 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.<ref name=:30/> In the case of gene silencing, various satellite RNA-based vectors can be used for sequence-specific inactivation.  [[Satellite tobacco mosaic virus|Satellite Tobacco Mosaic Virus]] (STMV) was the first subviral agent to be developed as a satellite virus-induced silencing system (SVISS).<ref name=:31>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.</ref>
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 cis-regulatory element|Bamboo mosaic virus satellite RNA]] (satBaMV),<ref name=":30">{{Cite journal |last=Lin |first=N S |last2=Lee |first2=Y S |last3=Lin |first3=B Y |last4=Lee |first4=C W |last5=Hsu |first5=Y H |date=April 2, 1996 |title=The open reading frame of bamboo mosaic potexvirus satellite RNA is not essential for its replication and can be replaced with a bacterial gene. |url=https://pnas.org/doi/full/10.1073/pnas.93.7.3138 |journal=Proceedings of the National Academy of Sciences |language=en |volume=93 |issue=7 |pages=3138–3142 |doi=10.1073/pnas.93.7.3138 |issn=0027-8424 |pmc=PMC39775 |pmid=8610182}}</ref> 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.<ref name=:30/> In the case of gene silencing, various satellite RNA-based vectors can be used for sequence-specific inactivation. [[Satellite tobacco mosaic virus|Satellite Tobacco Mosaic Virus]] (STMV) was the first subviral agent to be developed as a satellite virus-induced silencing system (SVISS).<ref name=":31">{{Cite journal |last=Gosselé |first=Véronique |last2=Faché |first2=Ina |last3=Meulewaeter |first3=Frank |last4=Cornelissen |first4=Marc |last5=Metzlaff |first5=Michael |date=December 2002 |title=SVISS - a novel transient gene silencing system for gene function discovery and validation in tobacco plants |url=http://doi.wiley.com/10.1046/j.1365-313X.2002.01471.x |journal=The Plant Journal |language=en |volume=32 |issue=5 |pages=859–866 |doi=10.1046/j.1365-313X.2002.01471.x}}</ref>


==References==
==References==

Revision as of 09:34, 26 February 2023

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, 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.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  4. ^ Alves, Carolina; Branco, Cristina; Cunha, Celso (2013). "Hepatitis Delta Virus: A Peculiar Virus". Advances in Virology. 2013: 1–11. doi:10.1155/2013/560105. ISSN 1687-8639. PMC 3807834. PMID 24198831.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  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. doi:10.1038/299316a0. ISSN 1476-4687.
  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.
  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.
  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.{{cite journal}}: CS1 maint: PMC format (link)
  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.{{cite journal}}: CS1 maint: PMC format (link)
  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.
  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.
  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.
  13. ^ Francki, R. I. B. (1987). Diener, T. O. (ed.). Possible Viroid Origin. Boston, MA: Springer US. pp. 205–218. doi:10.1007/978-1-4613-1855-2_9. ISBN 978-1-4612-9035-3. {{cite book}}: |work= ignored (help)
  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.
  15. ^ 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. doi:10.1094/MPMI-4-111. ISSN 0894-0282.
  16. ^ 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.{{cite journal}}: CS1 maint: PMC format (link)
  17. ^ 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. doi:10.1038/334265a0. ISSN 0028-0836.
  18. ^ 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.{{cite journal}}: CS1 maint: PMC format (link)
  19. ^ Diener, T. O. (August 1981). "Are viroids escaped introns?". Proceedings of the National Academy of Sciences. 78 (8): 5014–5015. doi:10.1073/pnas.78.8.5014. ISSN 0027-8424. PMC 320322. PMID 16593072.{{cite journal}}: CS1 maint: PMC format (link)
  20. ^ 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. doi:10.1073/pnas.83.17.6250. ISSN 0027-8424. PMC 386480. PMID 3462692.{{cite journal}}: CS1 maint: PMC format (link)
  21. ^ 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.
  22. ^ 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. doi:10.1073/pnas.83.1.58. ISSN 0027-8424. PMC 322790. PMID 3455758.{{cite journal}}: CS1 maint: PMC format (link)
  23. ^ Diener, T O (December 1989). "Circular RNAs: relics of precellular evolution?". Proceedings of the National Academy of Sciences. 86 (23): 9370–9374. doi:10.1073/pnas.86.23.9370. ISSN 0027-8424. PMC 298497. PMID 2480600.{{cite journal}}: CS1 maint: PMC format (link)
  24. ^ 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.
  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. Bibcode:2001JMolE..53..155E. doi:10.1007/s002390010203. PMID 11479686. S2CID 779074.
  26. ^ 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.{{cite journal}}: CS1 maint: PMC format (link)
  27. ^ 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.{{cite journal}}: CS1 maint: PMC format (link)
  28. ^ Litholdo, Celso Gaspar; da Fonseca, Guilherme Cordenonsi (2018). "Circular RNAs and Plant Stress Responses". In Xiao, Junjie (ed.). Circular RNAs. Vol. 1087. Singapore: Springer Singapore. pp. 345–353. doi:10.1007/978-981-13-1426-1_27. ISBN 978-981-13-1425-4.
  29. ^ 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.{{cite journal}}: CS1 maint: PMC format (link)
  30. ^ 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. doi:10.1186/1471-2148-10-97. ISSN 1471-2148. PMC 2858149. PMID 20377896.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
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External links

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