Broken, silent, and in hiding: tamed endogenous pararetroviruses escape elimination from the genome of sugar beet (Beta vulgaris).
Beta vulgaris
Caulimoviridae
Florendovirus
in situ hybridization
endogenous pararetrovirus
retrotransposon
sugar beet
Journal
Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347
Informations de publication
Date de publication:
26 08 2021
26 08 2021
Historique:
received:
04
03
2021
accepted:
16
03
2021
pubmed:
18
3
2021
medline:
28
9
2021
entrez:
17
3
2021
Statut:
ppublish
Résumé
Endogenous pararetroviruses (EPRVs) are widespread components of plant genomes that originated from episomal DNA viruses of the Caulimoviridae family. Due to fragmentation and rearrangements, most EPRVs have lost their ability to replicate through reverse transcription and to initiate viral infection. Similar to the closely related retrotransposons, extant EPRVs were retained and often amplified in plant genomes for several million years. Here, we characterize the complete genomic EPRV fraction of the crop sugar beet (Beta vulgaris, Amaranthaceae) to understand how they shaped the beet genome and to suggest explanations for their absent virulence. Using next- and third-generation sequencing data and genome assembly, we reconstructed full-length in silico representatives for the three host-specific EPRVs (beetEPRVs) in the B. vulgaris genome. Focusing on the endogenous caulimovirid beetEPRV3, we investigated its chromosomal localization, abundance and distribution by fluorescent in situ and Southern hybridization. Full-length beetEPRVs range between 7.5 and 10.7 kb in size, are heterogeneous in structure and sequence, and occupy about 0.3 % of the beet genome. Although all three beetEPRVs were assigned to the florendoviruses, they showed variably arranged protein-coding domains, different fragmentation, and preferences for diverse sequence contexts. We observed small RNAs that specifically target the individual beetEPRVs, indicating stringent epigenetic suppression. BeetEPRV3 sequences occur along all sugar beet chromosomes, preferentially in the vicinity of each other and are associated with heterochromatic, centromeric and intercalary satellite DNAs. BeetEPRV3 members also exist in genomes of related wild species, indicating an initial beetEPRV3 integration 13.4-7.2 million years ago. Our study in beet illustrates the variability of EPRV structure and sequence in a single host genome. Evidence of sequence fragmentation and epigenetic silencing implies possible plant strategies to cope with long-term persistence of EPRVs, including amplification, fixation in the heterochromatin, and containment of EPRV virulence.
Sections du résumé
BACKGROUND AND AIMS
Endogenous pararetroviruses (EPRVs) are widespread components of plant genomes that originated from episomal DNA viruses of the Caulimoviridae family. Due to fragmentation and rearrangements, most EPRVs have lost their ability to replicate through reverse transcription and to initiate viral infection. Similar to the closely related retrotransposons, extant EPRVs were retained and often amplified in plant genomes for several million years. Here, we characterize the complete genomic EPRV fraction of the crop sugar beet (Beta vulgaris, Amaranthaceae) to understand how they shaped the beet genome and to suggest explanations for their absent virulence.
METHODS
Using next- and third-generation sequencing data and genome assembly, we reconstructed full-length in silico representatives for the three host-specific EPRVs (beetEPRVs) in the B. vulgaris genome. Focusing on the endogenous caulimovirid beetEPRV3, we investigated its chromosomal localization, abundance and distribution by fluorescent in situ and Southern hybridization.
KEY RESULTS
Full-length beetEPRVs range between 7.5 and 10.7 kb in size, are heterogeneous in structure and sequence, and occupy about 0.3 % of the beet genome. Although all three beetEPRVs were assigned to the florendoviruses, they showed variably arranged protein-coding domains, different fragmentation, and preferences for diverse sequence contexts. We observed small RNAs that specifically target the individual beetEPRVs, indicating stringent epigenetic suppression. BeetEPRV3 sequences occur along all sugar beet chromosomes, preferentially in the vicinity of each other and are associated with heterochromatic, centromeric and intercalary satellite DNAs. BeetEPRV3 members also exist in genomes of related wild species, indicating an initial beetEPRV3 integration 13.4-7.2 million years ago.
CONCLUSIONS
Our study in beet illustrates the variability of EPRV structure and sequence in a single host genome. Evidence of sequence fragmentation and epigenetic silencing implies possible plant strategies to cope with long-term persistence of EPRVs, including amplification, fixation in the heterochromatin, and containment of EPRV virulence.
Identifiants
pubmed: 33729490
pii: 6174702
doi: 10.1093/aob/mcab042
pmc: PMC8389469
doi:
Substances chimiques
Retroelements
0
Sugars
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
281-299Commentaires et corrections
Type : CommentIn
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Références
BMC Genomics. 2004 Oct 18;5:80
pubmed: 15488154
Nucleic Acids Res. 2015 Jul 1;43(W1):W389-94
pubmed: 25883141
Sci Rep. 2018 Jan 12;8(1):572
pubmed: 29330451
Virus Res. 2019 Mar;262:48-53
pubmed: 29792903
Annu Rev Phytopathol. 2018 Aug 25;56:581-610
pubmed: 29979927
Genome Res. 2008 Mar;18(3):359-69
pubmed: 18256242
Plant Mol Biol. 2000 Jan;42(1):251-69
pubmed: 10688140
Genome Biol Evol. 2018 Oct 1;10(10):2686-2696
pubmed: 30239708
J Gen Virol. 2020 Feb;101(2):143-144
pubmed: 31958044
Mob DNA. 2013 Mar 01;4(1):8
pubmed: 23448600
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
Mol Biol Evol. 1988 Nov;5(6):675-90
pubmed: 2464735
Plant J. 2012 Dec;72(5):817-28
pubmed: 22900922
Biol Direct. 2009 Nov 02;4:41
pubmed: 19883502
Gene. 1991 May 30;101(2):247-50
pubmed: 2055488
Mol Gen Genet. 2000 Jul;263(6):908-15
pubmed: 10954075
J Virol. 2018 Apr 27;92(10):
pubmed: 29491164
DNA Res. 2023 Feb 1;30(1):
pubmed: 36208288
BMC Plant Biol. 2007 May 21;7:24
pubmed: 17517142
Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13241-6
pubmed: 10557305
Ann Bot. 2021 Jan 1;127(1):91-109
pubmed: 33009553
Plant J. 2018 May 23;:
pubmed: 29797366
Proc Natl Acad Sci U S A. 1984 Dec;81(24):8014-8
pubmed: 6096873
Virology. 2015 May;479-480:167-79
pubmed: 25677651
Ann Bot. 2016 Apr;117(4):625-41
pubmed: 26971286
Hum Mol Genet. 2013 Apr 1;22(7):1443-56
pubmed: 23297364
Bioinformatics. 2000 Feb;16(2):79-95
pubmed: 10842727
Trends Plant Sci. 2016 Sep;21(9):749-757
pubmed: 27427334
Theor Appl Genet. 1994 Aug;88(6-7):629-36
pubmed: 24186156
EMBO J. 2003 Sep 15;22(18):4836-45
pubmed: 12970195
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
J Gen Virol. 2000 Jun;81(Pt 6):1579-85
pubmed: 10811941
Plant J. 2014 Aug;79(3):385-97
pubmed: 24862340
Plant J. 2020 Jul;103(2):497-511
pubmed: 32100385
Nat Plants. 2018 Mar;4(3):136-137
pubmed: 29497160
BMC Plant Biol. 2009 Apr 08;9:42
pubmed: 19351415
Bioinformatics. 2013 Oct 1;29(19):2487-9
pubmed: 23842809
Trends Plant Sci. 2006 Oct;11(10):485-91
pubmed: 16949329
Bioinformatics. 2018 Oct 15;34(20):3575-3577
pubmed: 29762645
J Gen Virol. 2017 Feb;98(2):131-133
pubmed: 28284245
Mol Biol Evol. 1987 Jul;4(4):406-25
pubmed: 3447015
PLoS Biol. 2010 Mar 09;8(3):e1000326
pubmed: 20231873
Viruses. 2019 Aug 14;11(8):
pubmed: 31416187
Genome Res. 2006 Feb;16(2):251-9
pubmed: 16354755
Plant J. 2017 Jun;90(6):1156-1175
pubmed: 28257158
J Gen Virol. 2017 Apr;98(4):529-531
pubmed: 28452295
Chromosoma. 2011 Aug;120(4):409-22
pubmed: 21594600
Curr Opin Virol. 2013 Dec;3(6):615-20
pubmed: 24035682
FEBS Lett. 2020 Jun;594(12):1974-1988
pubmed: 32492176
Nat Commun. 2014 Nov 10;5:5269
pubmed: 25381880
Nat Plants. 2016 May 27;2(6):16074
pubmed: 27255838
Nature. 2014 Jan 23;505(7484):546-9
pubmed: 24352233
Theor Appl Genet. 1991 Oct;82(6):793-9
pubmed: 24213457
Plant J. 2014 Dec;80(5):823-33
pubmed: 25230921
J Virol. 2008 Jul;82(13):6697-710
pubmed: 18417582
PLoS Pathog. 2016 Nov 3;12(11):e1005819
pubmed: 27812219
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
EMBO J. 2000 Oct 16;19(20):5562-6
pubmed: 11032823
Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20140-5
pubmed: 24277848
EMBO J. 1990 Oct;9(10):3353-62
pubmed: 1698615
Int J Plant Genomics. 2009;2009:721091
pubmed: 19911065
Cell. 1998 Jun 26;93(7):1087-9
pubmed: 9657139
Mob DNA. 2020 Feb 4;11:8
pubmed: 32042316
BMC Bioinformatics. 2004 Aug 19;5:113
pubmed: 15318951
Virology. 1997 Sep 15;236(1):137-46
pubmed: 9299626
Virology. 2015 Feb;476:304-315
pubmed: 25576984
Nature. 2004 Sep 16;431(7006):364-70
pubmed: 15372044
J Gen Virol. 2020 Oct;101(10):1025-1026
pubmed: 32940596
J Gen Virol. 2018 Nov;99(11):1478-1479
pubmed: 30204080
Plant J. 2012 Nov;72(4):636-51
pubmed: 22804913
Plant J. 2012 Nov;72(4):600-11
pubmed: 22775355
Mol Plant Pathol. 2016 Dec;17(9):1317-1320
pubmed: 27870389
J Virol. 2013 Aug;87(15):8624-37
pubmed: 23720724
Nucleic Acids Res. 2011 Jan;39(Database issue):D70-4
pubmed: 21036865
Chromosome Res. 2010 Feb;18(2):247-63
pubmed: 20039119
Science. 1996 Nov 1;274(5288):765-8
pubmed: 8864112
J Virol. 2010 Jul;84(14):7346-59
pubmed: 20427523
Trends Plant Sci. 2003 Dec;8(12):570-5
pubmed: 14659705
Nucleic Acids Res. 1978 Sep;5(9):3231-6
pubmed: 704354
J Virol. 2018 May 29;92(12):
pubmed: 29618642
Arch Virol. 2010;155(1):123-31
pubmed: 19898772
Virology. 1999 Mar 15;255(2):207-13
pubmed: 10069945
Virology. 2015 May;479-480:2-25
pubmed: 25771806
Chromosome Res. 2006;14(8):881-97
pubmed: 17195925
Chromosome Res. 2009;17(3):379-96
pubmed: 19322668