Complete minicircle genome of Leptomonas pyrrhocoris reveals sources of its non-canonical mitochondrial RNA editing events.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
06 04 2021
Historique:
accepted: 09 02 2021
revised: 03 02 2021
received: 16 08 2020
pubmed: 5 3 2021
medline: 13 5 2021
entrez: 4 3 2021
Statut: ppublish

Résumé

Uridine insertion/deletion (U-indel) editing of mitochondrial mRNA, unique to the protistan class Kinetoplastea, generates canonical as well as potentially non-productive editing events. While the molecular machinery and the role of the guide (g) RNAs that provide required information for U-indel editing are well understood, little is known about the forces underlying its apparently error-prone nature. Analysis of a gRNA:mRNA pair allows the dissection of editing events in a given position of a given mitochondrial transcript. A complete gRNA dataset, paired with a fully characterized mRNA population that includes non-canonically edited transcripts, would allow such an analysis to be performed globally across the mitochondrial transcriptome. To achieve this, we have assembled 67 minicircles of the insect parasite Leptomonas pyrrhocoris, with each minicircle typically encoding one gRNA located in one of two similar-sized units of different origin. From this relatively narrow set of annotated gRNAs, we have dissected all identified mitochondrial editing events in L. pyrrhocoris, the strains of which dramatically differ in the abundance of individual minicircle classes. Our results support a model in which a multitude of editing events are driven by a limited set of gRNAs, with individual gRNAs possessing an inherent ability to guide canonical and non-canonical editing.

Identifiants

pubmed: 33660779
pii: 6154491
doi: 10.1093/nar/gkab114
pmc: PMC8034629
doi:

Substances chimiques

RNA, Guide 0
RNA, Messenger 0
RNA, Mitochondrial 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3354-3370

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

Eukaryot Cell. 2002 Aug;1(4):495-502
pubmed: 12455998
Emerg Infect Dis. 2019 Nov;25(11):2088-2092
pubmed: 31625841
J Clin Microbiol. 1999 May;37(5):1656-7
pubmed: 10328690
Nucleic Acids Res. 2018 Jan 25;46(2):765-781
pubmed: 29220521
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W540-3
pubmed: 15980530
Trends Genet. 2021 Feb;37(2):99-102
pubmed: 33203574
Cell. 1990 Nov 16;63(4):783-90
pubmed: 2171782
Nucleic Acids Res. 2009 Jul;37(Web Server issue):W202-8
pubmed: 19458158
Genes (Basel). 2019 Sep 26;10(10):
pubmed: 31561572
Wiley Interdiscip Rev RNA. 2016 Jan-Feb;7(1):33-51
pubmed: 26522170
Bioinformatics. 2006 Jul 1;22(13):1658-9
pubmed: 16731699
Biochemistry (Mosc). 2017 May;82(5):572-578
pubmed: 28601067
Nucleic Acids Res. 2017 Jul 27;45(13):7965-7983
pubmed: 28535252
Folia Parasitol (Praha). 2017 Jul 10;64:
pubmed: 28783029
PLoS One. 2017 Oct 26;12(10):e0185056
pubmed: 29073143
EMBO J. 1991 May;10(5):1217-24
pubmed: 1708723
Mol Biochem Parasitol. 2010 Oct;173(2):107-14
pubmed: 20546801
Cell. 1992 Aug 7;70(3):469-76
pubmed: 1379520
Cell. 1992 Aug 7;70(3):459-67
pubmed: 1379519
Mol Syst Biol. 2011 Oct 11;7:539
pubmed: 21988835
Nucleic Acids Res. 2019 Apr 23;47(7):3640-3657
pubmed: 30698753
J Cell Sci. 2004 Dec 15;117(Pt 26):6261-3
pubmed: 15591240
Cell. 1990 Jun 1;61(5):879-84
pubmed: 1693097
Sci Rep. 2016 Mar 29;6:23704
pubmed: 27021793
mBio. 2016 Mar 15;7(2):e01985
pubmed: 26980834
RNA. 2016 May;22(5):677-95
pubmed: 26908922
FEBS Lett. 1998 Jul 24;431(3):457-60
pubmed: 9714563
Nature. 2010 Dec 9;468(7325):784-9
pubmed: 21076397
PLoS One. 2008 Feb 13;3(2):e1566
pubmed: 18270563
RNA. 2010 Nov;16(11):2239-51
pubmed: 20855539
Genome Biol. 2004;5(2):R12
pubmed: 14759262
Mol Cell. 2016 Feb 4;61(3):364-378
pubmed: 26833087
Cell. 1990 Jun 15;61(6):1001-11
pubmed: 1693545
Exp Parasitol. 1999 Jul;92(3):215-8
pubmed: 10403763
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Wiley Interdiscip Rev RNA. 2018 Jun 11;:e1487
pubmed: 29888550
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Trends Genet. 2000 Jun;16(6):276-7
pubmed: 10827456
Trends Parasitol. 2020 Apr;36(4):337-355
pubmed: 32191849
Mol Biol Evol. 2016 Jun;33(6):1635-8
pubmed: 26921390
Proc Biol Sci. 1999 Mar 22;266(1419):611-20
pubmed: 10212451
Eukaryot Cell. 2004 Aug;3(4):862-9
pubmed: 15302819
Trends Parasitol. 2018 Jun;34(6):466-480
pubmed: 29605546
Mol Cell Biol. 1989 Mar;9(3):1365-7
pubmed: 2542768
Pathogens. 2020 Feb 05;9(2):
pubmed: 32033466
Nucleic Acids Res. 2014 Feb;42(3):1873-86
pubmed: 24174546
Nucleic Acids Res. 2017 May 5;45(8):4667-4686
pubmed: 28334821
Cell. 1991 Nov 1;67(3):537-46
pubmed: 1718605
Mol Biol (Mosk). 2001 Jan-Feb;35(1):3-13
pubmed: 11234380
Nucleic Acids Res. 1994 Apr 25;22(8):1489-95
pubmed: 7514788
Cell. 1990 Jan 26;60(2):189-98
pubmed: 1688737
Curr Mol Med. 2004 Sep;4(6):623-47
pubmed: 15357213
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
J Comput Biol. 2012 May;19(5):455-77
pubmed: 22506599
Annu Rev Microbiol. 2012;66:473-91
pubmed: 22994497
Nat Rev Mol Cell Biol. 2017 Nov;18(11):655-670
pubmed: 28951565
Eur J Protistol. 2012 Aug;48(3):185-93
pubmed: 22014411
Nucleic Acids Res. 2020 Mar 18;48(5):2694-2708
pubmed: 31919519
IUBMB Life. 2011 Jul;63(7):528-37
pubmed: 21698757
Nucleic Acids Res. 2020 Feb 20;48(3):1479-1493
pubmed: 31840176
Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):6986-93
pubmed: 10860961
PLoS Negl Trop Dis. 2015 Jul 23;9(7):e0003841
pubmed: 26204118
Folia Parasitol (Praha). 2000;47(1):1-5
pubmed: 10833008
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
mBio. 2015 Dec 01;6(6):e01498-15
pubmed: 26628723
PLoS Pathog. 2015 Aug 28;11(8):e1005127
pubmed: 26317207
Nucleic Acids Res. 2003 Jul 1;31(13):3672-8
pubmed: 12824391
RNA. 1995 Aug;1(6):634-43
pubmed: 7489522
Nucleic Acids Res. 2020 Sep 25;48(17):9747-9761
pubmed: 32853372
Wiley Interdiscip Rev RNA. 2018 Nov;9(6):e1502
pubmed: 30101566
Parasitology. 2019 Jan;146(1):1-27
pubmed: 29898792
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
Nucleic Acids Res. 2019 Dec 2;47(21):11304-11325
pubmed: 31665448

Auteurs

Evgeny S Gerasimov (ES)

Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.
Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow 119435, Russia.
Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127051, Russia.

Anna A Gasparyan (AA)

Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.

Dmitry A Afonin (DA)

Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.

Sara L Zimmer (SL)

Department of Biomedical Sciences, University of Minnesota Medical School, Duluth Campus, Duluth, MN 55812, USA.

Natalya Kraeva (N)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic.

Julius Lukeš (J)

Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice (Budweis), Czech Republic.
Faculty of Science, University of South Bohemia, 370 05 České Budějovice (Budweis), Czech Republic.

Vyacheslav Yurchenko (V)

Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow 119435, Russia.
Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic.

Alexander Kolesnikov (A)

Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH