A scenario for the emergence of protoviroids in the RNA world and for their further evolution into viroids and viroid-like RNAs by modular recombinations and mutations.
RNA evolution
hammerhead ribozyme
origin of life
rolling circle mechanism
satellite RNA
viroid-like RNA
Journal
Virus evolution
ISSN: 2057-1577
Titre abrégé: Virus Evol
Pays: England
ID NLM: 101664675
Informations de publication
Date de publication:
2022
2022
Historique:
received:
01
09
2021
revised:
10
12
2021
accepted:
14
01
2022
entrez:
28
2
2022
pubmed:
1
3
2022
medline:
1
3
2022
Statut:
epublish
Résumé
Viroids are tiny, circular, and noncoding RNAs that are able to replicate and systemically infect plants. The smallest known pathogens, viroids have been proposed to represent survivors from the RNA world that likely preceded the cellular world currently dominating life on the earth. Although the small, circular, and compact nature of viroid genomes, some of which are also endowed with catalytic activity mediated by hammerhead ribozymes, support this proposal, the lack of feasible evolutionary routes and the identification of hammerhead ribozymes in a large number of DNA genomes of organisms along the tree of life have led some to question such a proposal. Here, we reassess the origin and subsequent evolution of viroids by complementing phylogenetic reconstructions with molecular data, including the primary and higher-order structure of the genomic RNAs, their replication, and recombination mechanisms and selected biological information. Features of some viroid-like RNAs found in plants, animals, and possibly fungi are also considered. The resulting evolutionary scenario supports the emergence of protoviroids in the RNA world, mainly as replicative modules, followed by a further increase in genome complexity based on module/domain shuffling and combination and mutation. Such a modular evolutionary scenario would have facilitated the inclusion in the protoviroid genomes of complex RNA structures (or coding sequences, as in the case of hepatitis delta virus and delta-like agents), likely needed for their adaptation from the RNA world to a life based on cells, thus generating the ancestors of current infectious viroids and viroid-like RNAs. Other noninfectious viroid-like RNAs, such as retroviroid-like RNA elements and retrozymes, could also be derived from protoviroids if their reverse transcription and integration into viral or eukaryotic DNA, respectively, are considered as a possible key step in their evolution. Comparison of evidence supporting a general and modular evolutionary model for viroids and viroid-like RNAs with that favoring alternative scenarios provides reasonable reasons to keep alive the hypothesis that these small RNA pathogens may be relics of a precellular world.
Identifiants
pubmed: 35223083
doi: 10.1093/ve/veab107
pii: veab107
pmc: PMC8865084
doi:
Types de publication
Journal Article
Review
Langues
eng
Pagination
veab107Informations de copyright
© The Author(s) 2022. Published by Oxford University Press.
Références
Proc Natl Acad Sci U S A. 1985 Jul;82(14):4582-6
pubmed: 3860809
Cells. 2020 Nov 28;9(12):
pubmed: 33260527
Front Microbiol. 2020 Aug 18;11:1903
pubmed: 33013728
Proc Natl Acad Sci U S A. 1998 May 26;95(11):6560-5
pubmed: 9601006
Annu Rev Phytopathol. 2005;43:117-39
pubmed: 16078879
Virology. 1988 Feb;162(2):508-10
pubmed: 3341120
PLoS Pathog. 2020 Dec 22;16(12):e1009144
pubmed: 33351860
PLoS Pathog. 2014 Dec 11;10(12):e1004553
pubmed: 25503469
Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6792-7
pubmed: 15096616
Nucleic Acids Res. 1990 Jul 11;18(13):3998
pubmed: 2374724
Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11262-7
pubmed: 9326597
Cell Host Microbe. 2010 Jul 22;8(1):77-85
pubmed: 20638644
J Gen Virol. 1996 Nov;77 ( Pt 11):2839-46
pubmed: 8922479
Viruses. 2018 Dec 17;10(12):
pubmed: 30562970
Virus Res. 2015 Nov 2;209:136-45
pubmed: 25738582
Science. 1969 Dec 26;166(3913):1627-9
pubmed: 5352968
Proc Natl Acad Sci U S A. 2020 May 12;117(19):10126-10128
pubmed: 32317377
RNA. 1997 Jan;3(1):68-74
pubmed: 8990400
Virology. 2000 Mar 1;268(1):218-25
pubmed: 10683343
mBio. 2020 Mar 17;11(2):
pubmed: 32184255
J Gen Virol. 1993 Nov;74 ( Pt 11):2427-36
pubmed: 8245858
Genome Res. 2010 Dec;20(12):1700-10
pubmed: 20978141
Proc Natl Acad Sci U S A. 1980 Oct;77(10):6124-8
pubmed: 6934539
RNA. 2021 Sep;27(9):1017-1024
pubmed: 34131025
Nature. 1986 Oct 9-15;323(6088):508-14
pubmed: 3762705
Virus Evol. 2019 Jul 15;5(2):vez021
pubmed: 31321078
Virology. 1973 Sep;55(1):70-80
pubmed: 4728831
Curr Top Microbiol Immunol. 1999;239:81-105
pubmed: 9893370
J Virol. 1989 May;63(5):1945-50
pubmed: 2649689
Proc Natl Acad Sci U S A. 2017 Mar 21;114(12):E2401-E2410
pubmed: 28265094
RNA. 2010 Mar;16(3):463-73
pubmed: 20089682
J Gen Virol. 2001 Mar;82(Pt 3):687-691
pubmed: 11172112
Nature. 2001 Nov 1;414(6859):82-4
pubmed: 11689947
J Mol Evol. 2000 Jan;50(1):98-102
pubmed: 10654264
J Virol. 2012 Aug;86(15):8269-76
pubmed: 22623792
Plant Cell. 2016 May;28(5):1094-107
pubmed: 27113774
Nat Commun. 2019 May 8;10(1):2098
pubmed: 31068585
Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):424-9
pubmed: 10618434
Nat Rev Microbiol. 2019 Jul;17(7):449-458
pubmed: 31142823
Mol Plant Pathol. 2011 Sep;12(7):688-701
pubmed: 21726370
Sci Adv. 2015 Sep 25;1(8):e1500527
pubmed: 26601271
RNA Biol. 2017 Aug 3;14(8):985-991
pubmed: 28448743
PLoS One. 2014 Jan 30;9(1):e87297
pubmed: 24498066
mBio. 2019 Apr 2;10(2):
pubmed: 30940697
J Mol Biol. 1979 Sep 5;133(1):85-115
pubmed: 529284
J Gen Virol. 2001 Apr;82(Pt 4):953-962
pubmed: 11257203
Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12813-7
pubmed: 7809126
mBio. 2018 Nov 27;9(6):
pubmed: 30482837
J Virol. 2000 Aug;74(16):7204-10
pubmed: 10906174
Science. 1984 Feb 3;223(4635):450-5
pubmed: 6197756
Nature. 2007 Nov 15;450(7168):445-9
pubmed: 18004386
Nat New Biol. 1972 Jun 21;237(77):242-4
pubmed: 4504488
J Gen Virol. 2006 Jan;87(Pt 1):231-240
pubmed: 16361436
Curr Opin Struct Biol. 2004 Dec;14(6):757-64
pubmed: 15582400
Cell. 1987 Jul 3;50(1):9-16
pubmed: 3594567
Virus Res. 2020 Jun;282:197958
pubmed: 32277953
J Gen Virol. 1994 Apr;75 ( Pt 4):727-32
pubmed: 8151291
Nucleic Acids Res. 1992 Dec 11;20(23):6323-9
pubmed: 1282239
RNA. 2009 May;15(5):743-9
pubmed: 19318464
EMBO J. 2000 Jun 1;19(11):2662-70
pubmed: 10835363
Annu Rev Virol. 2021 Sep 29;8(1):305-325
pubmed: 34255541
RNA. 2007 Dec;13(12):2189-201
pubmed: 17956974
Proc Natl Acad Sci U S A. 1983 Oct;80(20):6234-8
pubmed: 6312450
Nucleic Acids Res. 2006;34(19):5613-22
pubmed: 17028097
Virology. 1980 Jul 15;104(1):1-9
pubmed: 18631656
J Virol. 1997 Sep;71(9):6603-10
pubmed: 9261382
RNA Biol. 2017 Aug 3;14(8):1046-1054
pubmed: 27574720
Virology. 1989 Jun;170(2):575-8
pubmed: 2728350
Cell. 1987 Feb 13;48(3):535-43
pubmed: 2433049
Nature. 1978 May 18;273(5659):203-8
pubmed: 643081
J Virol. 2018 Sep 26;92(20):
pubmed: 30068655
Nucleic Acids Res. 1989 Dec 11;17(23):10083-94
pubmed: 2602114
Nature. 1998 Oct 8;395(6702):567-74
pubmed: 9783582
EMBO J. 1994 Dec 15;13(24):6172-7
pubmed: 7813454
Biosci Rep. 1983 Aug;3(8):767-74
pubmed: 6626709
mBio. 2019 Apr 16;10(2):
pubmed: 30992348
Virology. 1979 Jul 15;96(1):47-53
pubmed: 18631591
Int J Mol Sci. 2021 Mar 28;22(7):
pubmed: 33800543
J Gen Virol. 1999 Aug;80 ( Pt 8):2239-2252
pubmed: 10466824
Nucleic Acids Res. 1987 Sep 11;15(17):7045-52
pubmed: 3658673
Proc Natl Acad Sci U S A. 2020 Jul 28;117(30):17977-17983
pubmed: 32651267
PLoS Pathog. 2017 Sep 14;13(9):e1006547
pubmed: 28910391
Virology. 1995 Jun 1;209(2):470-9
pubmed: 7539969
Nucleic Acids Res. 1991 Apr 25;19(8):1893-8
pubmed: 2030968
J Gen Virol. 2021 Feb;102(2):
pubmed: 33331814
mBio. 2016 Jun 14;7(3):
pubmed: 27302758
J Virol. 1998 Sep;72(9):7397-406
pubmed: 9696836
J Virol. 1987 Sep;61(9):2891-5
pubmed: 3612956
EMBO Rep. 2010 Sep;11(9):711-6
pubmed: 20651741
Nat Rev Microbiol. 2003 Oct;1(1):75-80
pubmed: 15040183
Viruses. 2009 Sep;1(2):241-54
pubmed: 21994548
J Gen Virol. 2013 Apr;94(Pt 4):711-719
pubmed: 23255620
J Gen Virol. 2017 Jul;98(7):1913-1922
pubmed: 28699864
Arch Virol. 2006 Aug;151(8):1539-49
pubmed: 16514498
Biol Direct. 2016 Mar 25;11(1):15
pubmed: 27016066
Mol Plant Pathol. 2014 Oct;15(8):767-79
pubmed: 25346967
Nucleic Acids Res. 1983 Sep 24;11(18):6185-97
pubmed: 6312412
Plant Cell. 2007 Nov;19(11):3610-26
pubmed: 18055612
Proc Natl Acad Sci U S A. 2012 Mar 6;109(10):3938-43
pubmed: 22345560
J Virol. 2011 Apr;85(7):3229-38
pubmed: 21270165
J Virol. 2003 Jun;77(11):6528-32
pubmed: 12743309
Science. 2009 Mar 6;323(5919):1308
pubmed: 19265013
Virus Res. 2018 Apr 2;249:8-15
pubmed: 29510173
RNA. 2012 May;18(5):871-85
pubmed: 22454536
PLoS Pathog. 2007 Nov;3(11):e182
pubmed: 18052530
Plant Mol Biol. 2003 Apr;51(6):991-9
pubmed: 12777056
Proc Natl Acad Sci U S A. 2020 May 12;117(19):10129-10130
pubmed: 32317376
Nature. 1988 Jul 21;334(6179):265-7
pubmed: 2456468
Nucleic Acids Res. 1981 Dec 11;9(23):6527-37
pubmed: 7322921
Nature. 1979 Mar 8;278(5700):185-8
pubmed: 763366
RNA Biol. 2016;13(1):83-97
pubmed: 26618399
Proc Natl Acad Sci U S A. 1988 Dec;85(23):9128-32
pubmed: 16594003
Science. 1996 Oct 4;274(5284):66-7
pubmed: 8848724
World J Gastroenterol. 2014 Mar 21;20(11):2971-8
pubmed: 24659888
Virology. 1972 Nov;50(2):606-9
pubmed: 4636118
Arch Virol. 2021 Nov;166(11):3157-3163
pubmed: 34396472
Proc Natl Acad Sci U S A. 1981 Aug;78(8):5014-5
pubmed: 16593072
Science. 1996 Oct 4;274(5284):90-4
pubmed: 8810253
Nucleic Acids Res. 1988 May 25;16(10):4197-216
pubmed: 2454454
Virus Genes. 1995;11(2-3):119-31
pubmed: 8828140
J Gen Virol. 1997 Jun;78 ( Pt 6):1207-11
pubmed: 9191909
Nucleic Acids Res. 2018 Nov 16;46(20):10563-10576
pubmed: 30304486
Viruses. 2019 May 09;11(5):
pubmed: 31075860
J Virol. 2000 Mar;74(6):2647-54
pubmed: 10684279
Proc Natl Acad Sci U S A. 1982 Oct;79(20):6285-8
pubmed: 16593239
J Gen Virol. 2009 Aug;90(Pt 8):2040-2049
pubmed: 19403756
Virus Evol. 2021 Feb 18;7(1):veab016
pubmed: 33708415
Proc Natl Acad Sci U S A. 1981 Nov;78(11):6932-5
pubmed: 6273895
J Mol Evol. 2001 Aug;53(2):155-9
pubmed: 11479686
Future Microbiol. 2010 Mar;5(3):393-402
pubmed: 20210550
Microbiol Rev. 1992 Jun;56(2):265-79
pubmed: 1620065
Arch Virol. 2009;154(6):993-7
pubmed: 19434474
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12709-14
pubmed: 12228725
Viruses. 2018 Nov 07;10(11):
pubmed: 30405008
Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6856-60
pubmed: 7542779
PLoS Pathog. 2006 Dec;2(12):e136
pubmed: 17196038
J Virol. 2005 Oct;79(20):12934-43
pubmed: 16188995
Proc Natl Acad Sci U S A. 1989 Dec;86(23):9370-4
pubmed: 2480600
Proc Natl Acad Sci U S A. 2012 Aug 21;109(34):13805-10
pubmed: 22869737
PLoS Genet. 2015 Jan 08;11(1):e1004906
pubmed: 25568943
Arch Virol. 2014 Mar;159(3):589-93
pubmed: 24077656
Virology. 1999 Jan 5;253(1):77-85
pubmed: 9887320
Virology. 2003 Sep 1;313(2):492-501
pubmed: 12954216
Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5631-4
pubmed: 1712103
RNA. 1998 Apr;4(4):418-29
pubmed: 9630248
Arch Virol. 2020 Oct;165(10):2177-2191
pubmed: 32748179
Nucleic Acids Res. 1997 Jul 15;25(14):2683-9
pubmed: 9207012
RNA. 2011 Jan;17(1):21-6
pubmed: 21081661
Proc Natl Acad Sci U S A. 1978 Feb;75(2):896-900
pubmed: 16592500
Virology. 1971 Jan;43(1):75-89
pubmed: 5543290
J Gen Virol. 2018 May;99(5):611-612
pubmed: 29580320
Gut. 1977 Dec;18(12):997-1003
pubmed: 75123
Plant J. 2012 Jun;70(6):991-1003
pubmed: 22332758
RNA Biol. 2019 Jul;16(7):906-917
pubmed: 30990352
Science. 2009 Nov 13;326(5955):953
pubmed: 19965505
Nucleic Acids Res. 1991 Dec 11;19(23):6640
pubmed: 1754400
Mol Plant Pathol. 2021 Feb;22(2):153-162
pubmed: 33305492
RNA. 2006 Dec;12(12):2126-34
pubmed: 17068206
Virology. 1971 Aug;45(2):411-28
pubmed: 5095900
Annu Rev Microbiol. 2014;68:395-414
pubmed: 25002087
RNA Biol. 2019 Mar;16(3):295-308
pubmed: 30734641
J Gen Virol. 2013 Mar;94(Pt 3):687-693
pubmed: 23152366
Proc Natl Acad Sci U S A. 1992 May 1;89(9):3711-5
pubmed: 1373888
Viruses. 2020 Mar 27;12(4):
pubmed: 32230827
Science. 1986 Mar 28;231(4745):1577-80
pubmed: 17833317
Virology. 2000 May 25;271(1):37-45
pubmed: 10814568
Virology. 1980 Jul 15;104(1):10-26
pubmed: 18631657
Genome Biol. 2016 Jun 23;17(1):135
pubmed: 27339130
RNA. 2005 Jul;11(7):1073-83
pubmed: 15928342
RNA. 2007 Jan;13(1):97-107
pubmed: 17105993
Semin Liver Dis. 2012 Aug;32(3):201-10
pubmed: 22932968
PLoS One. 2014 Jun 04;9(6):e98655
pubmed: 24897295
Virus Evol. 2021 Jan 25;7(1):veab001
pubmed: 33623708
Proc Natl Acad Sci U S A. 1986 Nov;83(22):8774-8
pubmed: 2430299
Mol Gen Genet. 1984;196(3):421-8
pubmed: 6094970
Science. 2020 Apr 10;368(6487):
pubmed: 32217750
Virus Res. 2003 Nov;97(2):145-9
pubmed: 14602207
Proc Natl Acad Sci U S A. 2019 Jun 25;116(26):13042-13050
pubmed: 31182602
Nucleic Acids Res. 1986 May 12;14(9):3627-40
pubmed: 3714492
Arch Virol. 2009;154(2):315-20
pubmed: 19112552