The Cassandra retrotransposon landscape in sugar beet (Beta vulgaris) and related Amaranthaceae: recombination and re-shuffling lead to a high structural variability.
Beta vulgaris (sugar beet)
Chenopodium quinoa (quinoa)
Cassandra
fluorescent in situ hybridization
long terminal repeat (LTR) retrotransposon
plant genomics
recombination
terminal-repeat retrotransposon in miniature (TRIM)
transposable element
Journal
Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347
Informations de publication
Date de publication:
01 01 2021
01 01 2021
Historique:
received:
28
09
2020
accepted:
28
09
2020
pubmed:
4
10
2020
medline:
28
1
2021
entrez:
3
10
2020
Statut:
ppublish
Résumé
Plant genomes contain many retrotransposons and their derivatives, which are subject to rapid sequence turnover. As non-autonomous retrotransposons do not encode any proteins, they experience reduced selective constraints leading to their diversification into multiple families, usually limited to a few closely related species. In contrast, the non-coding Cassandra terminal repeat retrotransposons in miniature (TRIMs) are widespread in many plants. Their hallmark is a conserved 5S rDNA-derived promoter in their long terminal repeats (LTRs). As sugar beet (Beta vulgaris) has a well-described LTR retrotransposon landscape, we aim to characterize TRIMs in beet and related genomes. We identified Cassandra retrotransposons in the sugar beet reference genome and characterized their structural relationships. Genomic organization, chromosomal localization, and distribution of Cassandra-TRIMs across the Amaranthaceae were verified by Southern and fluorescent in situ hybridization. All 638 Cassandra sequences in the sugar beet genome contain conserved LTRs and thus constitute a single family. Nevertheless, variable internal regions required a subdivision into two Cassandra subfamilies within B. vulgaris. The related Chenopodium quinoa harbours a third subfamily. These subfamilies vary in their distribution within Amaranthaceae genomes, their insertion times and the degree of silencing by small RNAs. Cassandra retrotransposons gave rise to many structural variants, such as solo LTRs or tandemly arranged Cassandra retrotransposons. These Cassandra derivatives point to an interplay of template switch and recombination processes - mechanisms that likely caused Cassandra's subfamily formation and diversification. We traced the evolution of Cassandra in the Amaranthaceae and detected a considerable variability within the short internal regions, whereas the LTRs are strongly conserved in sequence and length. Presumably these hallmarks make Cassandra a prime target for unequal recombination, resulting in the observed structural diversity, an example of the impact of LTR-mediated evolutionary mechanisms on the host genome.
Sections du résumé
BACKGROUND AND AIMS
Plant genomes contain many retrotransposons and their derivatives, which are subject to rapid sequence turnover. As non-autonomous retrotransposons do not encode any proteins, they experience reduced selective constraints leading to their diversification into multiple families, usually limited to a few closely related species. In contrast, the non-coding Cassandra terminal repeat retrotransposons in miniature (TRIMs) are widespread in many plants. Their hallmark is a conserved 5S rDNA-derived promoter in their long terminal repeats (LTRs). As sugar beet (Beta vulgaris) has a well-described LTR retrotransposon landscape, we aim to characterize TRIMs in beet and related genomes.
METHODS
We identified Cassandra retrotransposons in the sugar beet reference genome and characterized their structural relationships. Genomic organization, chromosomal localization, and distribution of Cassandra-TRIMs across the Amaranthaceae were verified by Southern and fluorescent in situ hybridization.
KEY RESULTS
All 638 Cassandra sequences in the sugar beet genome contain conserved LTRs and thus constitute a single family. Nevertheless, variable internal regions required a subdivision into two Cassandra subfamilies within B. vulgaris. The related Chenopodium quinoa harbours a third subfamily. These subfamilies vary in their distribution within Amaranthaceae genomes, their insertion times and the degree of silencing by small RNAs. Cassandra retrotransposons gave rise to many structural variants, such as solo LTRs or tandemly arranged Cassandra retrotransposons. These Cassandra derivatives point to an interplay of template switch and recombination processes - mechanisms that likely caused Cassandra's subfamily formation and diversification.
CONCLUSIONS
We traced the evolution of Cassandra in the Amaranthaceae and detected a considerable variability within the short internal regions, whereas the LTRs are strongly conserved in sequence and length. Presumably these hallmarks make Cassandra a prime target for unequal recombination, resulting in the observed structural diversity, an example of the impact of LTR-mediated evolutionary mechanisms on the host genome.
Identifiants
pubmed: 33009553
pii: 5917450
doi: 10.1093/aob/mcaa176
pmc: PMC7750724
doi:
Substances chimiques
Retroelements
0
Sugars
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
91-109Informations de copyright
© The Author(s) 2020. 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
Proc Natl Acad Sci U S A. 2003 May 27;100(11):6569-74
pubmed: 12743378
Curr Opin Plant Biol. 2015 Oct;27:67-76
pubmed: 26164237
Sci Rep. 2015 Dec 03;5:17644
pubmed: 26631625
Genome Biol Evol. 2014 Jun 04;6(6):1423-36
pubmed: 24899073
Genome Res. 2003 Sep;13(9):1984-97
pubmed: 12952871
PLoS One. 2012;7(2):e32010
pubmed: 22359654
Mob DNA. 2013 Mar 01;4(1):8
pubmed: 23448600
Appl Plant Sci. 2016 Aug 05;4(8):
pubmed: 27610279
Plant Mol Biol. 2001 Jan;45(1):113-22
pubmed: 11247602
Genes Dev. 2015 Jun 15;29(12):1256-70
pubmed: 26109049
Plant J. 2016 May;86(3):268-85
pubmed: 26996788
Genome Biol Evol. 2015 Jan 07;7(2):493-504
pubmed: 25573958
BMC Genomics. 2016 Dec 6;17(1):997
pubmed: 27919246
Plant J. 2020 Feb;101(3):681-699
pubmed: 31610059
Proc Natl Acad Sci U S A. 1984 Dec;81(24):8014-8
pubmed: 6096873
Genome Biol. 2018 Nov 19;19(1):199
pubmed: 30454069
BMC Genomics. 2007 Jul 06;8:218
pubmed: 17617907
Genome Res. 2018 May;28(5):714-725
pubmed: 29588362
Arch Virol. 2001;146(11):2255-61
pubmed: 11765927
Theor Appl Genet. 1994 Aug;88(6-7):629-36
pubmed: 24186156
Nat Commun. 2012 May 22;3:854
pubmed: 22617294
Plant Mol Biol. 2012 Mar;78(4-5):393-405
pubmed: 22246381
Nature. 2010 Apr 29;464(7293):1347-50
pubmed: 20428170
Genome Biol Evol. 2019 Dec 1;11(12):3382-3392
pubmed: 31755923
Ann Bot. 2005 Jan;95(1):127-32
pubmed: 15596462
Plant J. 2014 Aug;79(3):385-97
pubmed: 24862340
G3 (Bethesda). 2015 May 26;5(8):1585-92
pubmed: 26019188
Bioinformatics. 2013 Oct 1;29(19):2487-9
pubmed: 23842809
Front Plant Sci. 2020 May 20;11:644
pubmed: 32508870
Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13778-83
pubmed: 11717436
Proc Natl Acad Sci U S A. 2013 Jan 15;110(3):1012-6
pubmed: 23277587
Nat Genet. 1998 Sep;20(1):43-5
pubmed: 9731528
Theor Appl Genet. 2007 Feb;114(4):627-36
pubmed: 17160537
Bioinformatics. 2018 Oct 15;34(20):3575-3577
pubmed: 29762645
Science. 1990 Nov 30;250(4985):1227-33
pubmed: 1700865
Nat Commun. 2017 May 24;8:15275
pubmed: 28537264
Nat Rev Genet. 2008 May;9(5):397-405
pubmed: 18368054
Genome Biol Evol. 2013;5(5):954-65
pubmed: 23426643
Mol Biol Evol. 1987 Jul;4(4):406-25
pubmed: 3447015
Nature. 2004 Jul 22;430(6998):471-6
pubmed: 15269773
Nat Commun. 2017 Nov 3;8(1):1283
pubmed: 29097664
Cytogenet Genome Res. 2005;110(1-4):441-7
pubmed: 16093696
J Mol Evol. 2005 Sep;61(3):275-91
pubmed: 16034651
Chromosoma. 2011 Aug;120(4):409-22
pubmed: 21594600
Mol Ecol Resour. 2018 Nov;18(6):1188-1195
pubmed: 30035372
Plant J. 2010 Aug;63(4):584-98
pubmed: 20525006
Nature. 2014 Jan 23;505(7484):546-9
pubmed: 24352233
Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):383-8
pubmed: 16381819
Genome Res. 2004 May;14(5):860-9
pubmed: 15078861
Nat Rev Genet. 2007 Apr;8(4):272-85
pubmed: 17363976
Trends Ecol Evol. 2010 Sep;25(9):537-46
pubmed: 20591532
BMC Plant Biol. 2010 Jan 11;10:8
pubmed: 20064260
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
Theor Appl Genet. 2006 Apr;112(6):999-1008
pubmed: 16404583
Nat Genet. 2003 Sep;35(1):41-8
pubmed: 12897783
Cytogenet Genome Res. 2005;110(1-4):91-107
pubmed: 16093661
BMC Genomics. 2012 Apr 16;13:137
pubmed: 22507400
Curr Opin Virol. 2013 Dec;3(6):604-14
pubmed: 24035277
Nat Rev Genet. 2013 Jan;14(1):49-61
pubmed: 23247435
Nat Rev Genet. 2011 May 04;12(7):459-63
pubmed: 21540878
PLoS One. 2016 Oct 5;11(10):e0163962
pubmed: 27706213
Nat Rev Genet. 2017 Feb;18(2):71-86
pubmed: 27867194
DNA Res. 2016 Dec;23(6):535-546
pubmed: 27458999
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Curr Opin Genet Dev. 2018 Apr;49:15-24
pubmed: 29505963
FEMS Yeast Res. 2011 Jun;11(4):334-44
pubmed: 21272231
Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5833-8
pubmed: 18408163
J Virol. 2000 Nov;74(22):10819-21
pubmed: 11044130
Gene. 2008 Jan 15;407(1-2):75-85
pubmed: 17976929
Genomics. 2009 May;93(5):494-500
pubmed: 19442632
Genome Biol. 2004;5(6):225
pubmed: 15186483
Plant J. 2016 Jan;85(2):229-44
pubmed: 26676716
Genetics. 2004 Mar;166(3):1437-50
pubmed: 15082561
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17638-43
pubmed: 17101966
PLoS Genet. 2013 Nov;9(11):e1003922
pubmed: 24244190
Gene. 2015 May 1;561(2):283-91
pubmed: 25701601
Nature. 2017 Feb 16;542(7641):307-312
pubmed: 28178233
Genome Res. 2016 Feb;26(2):226-37
pubmed: 26631490
Plant J. 2012 Nov;72(4):636-51
pubmed: 22804913
J Virol. 1990 Sep;64(9):4321-8
pubmed: 1696639
Proc Natl Acad Sci U S A. 2012 Apr 10;109(15):5880-5
pubmed: 22451936
Int J Mol Sci. 2020 Apr 22;21(8):
pubmed: 32331257
Biochem J. 2003 May 1;371(Pt 3):641-51
pubmed: 12564956
BMC Plant Biol. 2012 Jun 20;12:95
pubmed: 22716941
Genome Res. 2002 Jul;12(7):1075-9
pubmed: 12097344
Genome Biol. 2016 Jan 18;17:7
pubmed: 26781660
Annu Rev Genet. 1999;33:479-532
pubmed: 10690416
BMC Genomics. 2010 Jun 29;11:408
pubmed: 20584339
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Chromosome Res. 2010 Feb;18(2):247-63
pubmed: 20039119
Mol Biol Evol. 2016 Jul;33(7):1870-4
pubmed: 27004904
Science. 1996 Nov 1;274(5288):765-8
pubmed: 8864112
BMC Genomics. 2007 Jul 24;8:247
pubmed: 17650302
Philos Trans R Soc Lond B Biol Sci. 2017 Dec 19;372(1736):
pubmed: 29109221
Curr Opin Genet Dev. 2005 Dec;15(6):621-7
pubmed: 16219458
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Chromosome Res. 2015 Sep;23(3):583-96
pubmed: 26293606
Mob DNA. 2010 Mar 08;1(1):11
pubmed: 20226008
Mol Cell. 2015 Dec 3;60(5):715-727
pubmed: 26585389
J Hered. 2002 Jan-Feb;93(1):77-8
pubmed: 12011185
Nat Rev Genet. 2007 Dec;8(12):973-82
pubmed: 17984973
Mol Biol Evol. 2000 Oct;17(10):1483-98
pubmed: 11018155
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):E981-8
pubmed: 22460791
Chromosome Res. 2009;17(3):379-96
pubmed: 19322668
Mol Genet Genomics. 2004 Dec;272(5):504-11
pubmed: 15503144
BMC Genomics. 2013 Mar 04;14:142
pubmed: 23452340