A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants.
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
11 10 2021
11 10 2021
Historique:
accepted:
17
09
2021
revised:
17
08
2021
received:
03
06
2021
pubmed:
28
9
2021
medline:
28
12
2021
entrez:
27
9
2021
Statut:
ppublish
Résumé
Pervasive transcription of eukaryotic genomes results in expression of long non-coding RNAs (lncRNAs) most of which are poorly conserved in evolution and appear to be non-functional. However, some lncRNAs have been shown to perform specific functions, in particular, transcription regulation. Thousands of small open reading frames (smORFs, <100 codons) located on lncRNAs potentially might be translated into peptides or microproteins. We report a comprehensive analysis of the conservation and evolutionary trajectories of lncRNAs-smORFs from the moss Physcomitrium patens across transcriptomes of 479 plant species. Although thousands of smORFs are subject to substantial purifying selection, the majority of the smORFs appear to be evolutionary young and could represent a major pool for functional innovation. Using nanopore RNA sequencing, we show that, on average, the transcriptional level of conserved smORFs is higher than that of non-conserved smORFs. Proteomic analysis confirmed translation of 82 novel species-specific smORFs. Numerous conserved smORFs containing low complexity regions (LCRs) or transmembrane domains were identified, the biological functions of a selected LCR-smORF were demonstrated experimentally. Thus, microproteins encoded by smORFs are a major, functionally diverse component of the plant proteome.
Identifiants
pubmed: 34570232
pii: 6376030
doi: 10.1093/nar/gkab816
pmc: PMC8501992
doi:
Substances chimiques
Proteome
0
RNA, Long Noncoding
0
Types de publication
Journal Article
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
10328-10346Informations de copyright
Published by Oxford University Press on behalf of Nucleic Acids Research 2021.
Références
PLoS One. 2013 Sep 27;8(9):e77356
pubmed: 24086772
Nat Methods. 2015 Feb;12(2):147-53
pubmed: 25486063
Genomics. 2020 Mar;112(2):1120-1127
pubmed: 31247329
J Mol Evol. 1980 Dec;16(2):111-20
pubmed: 7463489
Nature. 2019 Oct;574(7780):679-685
pubmed: 31645766
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Mol Cell Biol. 2020 Feb 27;40(6):
pubmed: 31907280
G3 (Bethesda). 2019 Aug 8;9(8):2511-2520
pubmed: 31235560
Nature. 2007 Jun 14;447(7146):799-816
pubmed: 17571346
BMC Bioinformatics. 2020 Oct 14;21(1):455
pubmed: 33054771
Front Plant Sci. 2020 Mar 12;11:276
pubmed: 32226437
Science. 2007 Jun 8;316(5830):1484-8
pubmed: 17510325
J Proteome Res. 2014 Mar 7;13(3):1757-65
pubmed: 24490786
Nat Protoc. 2012 Jul 26;7(8):1534-50
pubmed: 22836135
BMC Bioinformatics. 2014 Nov 21;15:380
pubmed: 25413677
Nat Ecol Evol. 2017 Jun;1(6):0146-146
pubmed: 28642936
Nat Rev Microbiol. 2014 Sep;12(9):647-53
pubmed: 25069631
Genome Biol. 2017 Aug 30;18(1):162
pubmed: 28854954
Curr Biol. 2018 Aug 6;28(15):2365-2376.e5
pubmed: 30033333
PLoS Comput Biol. 2013;9(2):e1002917
pubmed: 23468607
BMC Genomics. 2009 Apr 16;10:162
pubmed: 19371439
Trends Genet. 2000 Jun;16(6):276-7
pubmed: 10827456
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W116-20
pubmed: 15980438
Elife. 2021 Feb 17;10:
pubmed: 33594971
Cell Cycle. 2020 Jul;19(14):1777-1785
pubmed: 32594847
Cell Rep. 2021 Mar 9;34(10):108815
pubmed: 33691108
EMBO J. 2020 Sep 1;39(17):e104763
pubmed: 32744758
Bioinformatics. 2002 Dec;18(12):1703-4
pubmed: 12490463
Plant J. 2018 Feb;93(3):515-533
pubmed: 29237241
Mol Plant Pathol. 2021 Jan;22(1):77-91
pubmed: 33146443
Trends Genet. 2017 Aug;33(8):540-552
pubmed: 28629949
Nat Methods. 2014 Nov;11(11):1114-25
pubmed: 25357241
Hum Mol Genet. 2002 Mar 15;11(6):669-74
pubmed: 11912182
Genome Res. 2012 Mar;22(3):577-91
pubmed: 22110045
Elife. 2014 Aug 21;3:e03528
pubmed: 25144939
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Curr Protoc Plant Biol. 2019 Sep;4(3):e20098
pubmed: 31479208
Front Plant Sci. 2015 Jul 20;6:544
pubmed: 26257754
Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36
pubmed: 7584402
Bioinformatics. 2016 Jul 15;32(14):2103-10
pubmed: 27153593
Nat Methods. 2020 Mar;17(3):261-272
pubmed: 32015543
Elife. 2015 Dec 19;4:e08890
pubmed: 26687005
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12
pubmed: 16845082
Mol Biol Evol. 2015 May;32(5):1365-71
pubmed: 25701167
Genome Biol. 2011 Nov 25;12(11):R118
pubmed: 22118156
BMC Evol Biol. 2012 Aug 24;12:155
pubmed: 22920595
IEEE Trans Vis Comput Graph. 2014 Dec;20(12):1983-92
pubmed: 26356912
Genome Biol. 2015 Sep 14;16:179
pubmed: 26364619
Mol Biol Evol. 2018 Mar 1;35(3):631-645
pubmed: 29220506
Genome Res. 2019 Sep;29(9):1464-1477
pubmed: 31387879
Methods Mol Biol. 2019;1933:415-429
pubmed: 30945201
Nat Biotechnol. 2019 Apr;37(4):420-423
pubmed: 30778233
BMC Plant Biol. 2019 Jan 7;19(1):9
pubmed: 30616513
Plants (Basel). 2020 Dec 17;9(12):
pubmed: 33348863
Mol Plant. 2020 Jul 6;13(7):1078-1093
pubmed: 32445888
Science. 2020 Mar 6;367(6482):1140-1146
pubmed: 32139545
Nat Chem Biol. 2013 Jan;9(1):59-64
pubmed: 23160002
Methods Mol Biol. 2019;1933:397-414
pubmed: 30945200
Elife. 2020 Jan 14;9:
pubmed: 31931956
Nature. 2011 Feb 10;470(7333):284-8
pubmed: 21307942
Gene. 2017 Apr 30;610:103-111
pubmed: 28185860
Nucleic Acids Res. 2019 Jan 8;47(D1):D442-D450
pubmed: 30395289
Cell. 2019 Jun 27;178(1):242-260.e29
pubmed: 31155234
J Mol Evol. 2020 May;88(4):382-398
pubmed: 32253450
Elife. 2017 Jun 05;6:
pubmed: 28580901
Mol Biol Evol. 2012 Mar;29(3):883-6
pubmed: 22045997
PLoS Genet. 2010 Sep 09;6(9):e1001115
pubmed: 20838599
Cell Rep. 2015 May 19;11(7):1110-22
pubmed: 25959816
Cell. 2019 Aug 22;178(5):1245-1259.e14
pubmed: 31402174
Genome Biol. 2019 Dec 16;20(1):278
pubmed: 31842956
Nat Protoc. 2016 Dec;11(12):2301-2319
pubmed: 27809316
Brief Bioinform. 2018 Jul 20;19(4):636-643
pubmed: 28137767
Plant Cell. 2015 Aug;27(8):2095-118
pubmed: 26276833
Nature. 2012 Jul 19;487(7407):370-4
pubmed: 22722833
F1000Res. 2020 Apr 28;9:304
pubmed: 32489650
Nat Commun. 2020 Mar 18;11(1):1438
pubmed: 32188845
Nat Ecol Evol. 2018 May;2(5):890-896
pubmed: 29556078
Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):E10018-E10027
pubmed: 29087317
Noncoding RNA. 2020 Sep 23;6(4):
pubmed: 32977531
Nat Commun. 2020 Feb 7;11(1):781
pubmed: 32034123
Curr Protein Pept Sci. 2011 Aug;12(5):399-408
pubmed: 21418016
NAR Genom Bioinform. 2019 Jul 05;1(1):e2
pubmed: 33575549
BMC Bioinformatics. 2017 Jan 17;18(1):37
pubmed: 28095775
Mol Biol Evol. 2010 Aug;27(8):1745-9
pubmed: 20360214
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Nature. 2020 Mar;579(7799):409-414
pubmed: 32188942
PLoS Comput Biol. 2017 Mar 29;13(3):e1005375
pubmed: 28355220
Nucleic Acids Res. 2014 Jun;42(11):7132-44
pubmed: 24792168
Nat Plants. 2020 Oct;6(10):1262-1274
pubmed: 32958895
Nucleic Acids Res. 2020 Aug 20;48(14):7700-7711
pubmed: 32652016
J Mol Biol. 2001 Jan 19;305(3):567-80
pubmed: 11152613
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
pubmed: 9254694
Cell. 2018 Jan 25;172(3):393-407
pubmed: 29373828
Curr Protoc Bioinformatics. 2014 Sep 08;47:11.12.1-34
pubmed: 25199790
Methods Mol Biol. 2007;355:9-14
pubmed: 17093297
Nat Rev Mol Cell Biol. 2017 Sep;18(9):575-589
pubmed: 28698598
Nat Rev Genet. 2016 Oct;17(10):601-14
pubmed: 27573374
Elife. 2020 Oct 28;9:
pubmed: 33112233
Brief Bioinform. 2019 Sep 27;20(5):1853-1864
pubmed: 30010717
Exp Cell Res. 2020 Aug 1;393(1):112057
pubmed: 32387289
Nat Rev Genet. 2015 Jul;16(7):409-20
pubmed: 26055156
Nature. 2015 Apr 2;520(7545):90-3
pubmed: 25807486
Genome Res. 2020 Oct;30(10):1418-1433
pubmed: 32973042
Sci Rep. 2016 Mar 01;6:22352
pubmed: 26925972
PLoS Genet. 2019 May 23;15(5):e1008160
pubmed: 31120894
J Exp Bot. 2015 Aug;66(17):5337-49
pubmed: 26071531
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Methods Enzymol. 1996;266:554-71
pubmed: 8743706
Nat Chem Biol. 2020 Apr;16(4):458-468
pubmed: 31819274
Mol Syst Biol. 2019 Feb 22;15(2):e8290
pubmed: 30796087
RNA. 2016 Jun;22(6):867-82
pubmed: 27090285
BMC Genomics. 2018 May 29;19(1):414
pubmed: 29843593
Nature. 2020 Dec;588(7838):503-508
pubmed: 33299178
Cell. 2020 Nov 25;183(5):1151-1161
pubmed: 33068526
Annu Rev Cell Dev Biol. 2019 Oct 6;35:407-431
pubmed: 31403819
Nucleic Acids Res. 2018 Jan 4;46(D1):D497-D502
pubmed: 29140531
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Nature. 2017 Jan 12;541(7636):228-232
pubmed: 28024296
Elife. 2019 Nov 01;8:
pubmed: 31674305
Plant Physiol. 2017 Oct;175(2):619-627
pubmed: 28807931
BMC Bioinformatics. 2019 Nov 8;20(1):559
pubmed: 31703551