A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants

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. Thousan...

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Vydáno v:Nucleic acids research Ročník 49; číslo 18; s. 10328 - 10346
Hlavní autoři: Fesenko, Igor, Shabalina, Svetlana A, Mamaeva, Anna, Knyazev, Andrey, Glushkevich, Anna, Lyapina, Irina, Ziganshin, Rustam, Kovalchuk, Sergey, Kharlampieva, Daria, Lazarev, Vassili, Taliansky, Michael, Koonin, Eugene V
Médium: Journal Article
Jazyk:angličtina
Vydáno: England Oxford University Press 11.10.2021
Témata:
Bryopsida - genetics
Computational Biology
Open Reading Frames
Proteome
RNA, Long Noncoding
Transcriptome
ISSN:0305-1048, 1362-4962, 1362-4962
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Abstract 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.
AbstractList 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.
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.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.
Author Fesenko, Igor
Koonin, Eugene V
Shabalina, Svetlana A
Knyazev, Andrey
Taliansky, Michael
Ziganshin, Rustam
Mamaeva, Anna
Kharlampieva, Daria
Kovalchuk, Sergey
Lazarev, Vassili
Lyapina, Irina
Glushkevich, Anna
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  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
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  givenname: Svetlana A
  orcidid: 0000-0002-3774-819X
  surname: Shabalina
  fullname: Shabalina, Svetlana A
  organization: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA
– sequence: 3
  givenname: Anna
  surname: Mamaeva
  fullname: Mamaeva, Anna
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
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  givenname: Andrey
  surname: Knyazev
  fullname: Knyazev, Andrey
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
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  surname: Glushkevich
  fullname: Glushkevich, Anna
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
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  givenname: Irina
  surname: Lyapina
  fullname: Lyapina, Irina
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
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  givenname: Rustam
  surname: Ziganshin
  fullname: Ziganshin, Rustam
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
– sequence: 8
  givenname: Sergey
  surname: Kovalchuk
  fullname: Kovalchuk, Sergey
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation
– sequence: 9
  givenname: Daria
  surname: Kharlampieva
  fullname: Kharlampieva, Daria
  organization: Department of Cell Biology, Federal Research and Clinical Center of Physical -Chemical Medicine of Federal Medical Biological Agency, Moscow 119435, Russian Federation
– sequence: 10
  givenname: Vassili
  surname: Lazarev
  fullname: Lazarev, Vassili
  organization: Department of Cell Biology, Federal Research and Clinical Center of Physical -Chemical Medicine of Federal Medical Biological Agency, Moscow 119435, Russian Federation, Moscow Institute of Physics and Technology (National Research University), Dolgoprudny, Moscow region, 141701, Russian Federation
– sequence: 11
  givenname: Michael
  surname: Taliansky
  fullname: Taliansky, Michael
  organization: Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russian Federation, The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
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  givenname: Eugene V
  orcidid: 0000-0003-3943-8299
  surname: Koonin
  fullname: Koonin, Eugene V
  organization: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA
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Cites_doi 10.1016/j.cell.2020.09.047
10.1002/cppb.20098
10.1006/jmbi.2000.4315
10.1093/nar/gki442
10.15252/msb.20188290
10.1093/nar/gkl315
10.1038/nature09701
10.1093/bioinformatics/btw152
10.4081/eb.2012.e7
10.1186/s13059-015-0742-x
10.1186/gb-2011-12-11-r118
10.7554/eLife.59303
10.1016/j.ygeno.2019.06.026
10.1186/1471-2164-10-162
10.1038/nmeth.3144
10.3390/plants9121794
10.1016/S0168-9525(00)02024-2
10.7554/eLife.47014
10.1038/nchembio.1120
10.1186/s12859-016-1458-y
10.1038/srep22352
10.1093/nargab/lqz002
10.1016/j.celrep.2021.108815
10.1093/molbev/msu300
10.1016/0097-8485(93)85006-X
10.1186/s12859-019-3033-9
10.1038/s41587-019-0036-z
10.1038/s41467-020-14500-z
10.1038/s41586-020-2094-2
10.1126/science.aay0262
10.1111/tpj.13801
10.1007/978-3-030-31964-9_16
10.1101/gr.253302.119
10.1186/s13059-019-1910-1
10.7554/eLife.03528
10.7554/eLife.53734
10.1101/gr.133009.111
10.1016/j.gene.2017.02.004
10.1080/15384101.2020.1779470
10.1093/hmg/11.6.669
10.1038/nrg.2016.85
10.1016/j.cell.2019.07.016
10.1038/s41592-019-0686-2
10.1093/nar/25.17.3389
10.1109/TVCG.2014.2346248
10.1186/s12859-020-03805-x
10.1007/978-1-4939-9045-0_26
10.1016/j.molp.2020.05.012
10.1186/1471-2148-12-155
10.7554/eLife.49658
10.1186/s12864-018-4765-z
10.1093/molbev/msq086
10.1038/nmeth.3208
10.7554/eLife.08890
10.12688/f1000research.23297.1
10.1101/gr.261834.120
10.21105/joss.03021
10.1038/nature11184
10.1385/1-59259-192-2:301
10.1093/bioinformatics/btt656
10.1371/journal.pone.0077356
10.1016/j.celrep.2015.04.023
10.1038/s41586-020-3021-2
10.2174/138920311796391106
10.1038/s41589-019-0425-0
10.1371/journal.pcbi.1002917
10.1093/nar/gku342
10.1038/s41586-019-1693-2
10.1016/j.cell.2019.05.010
10.1093/nar/gkx1130
10.1111/mpp.13009
10.1371/journal.pcbi.1005375
10.3102/10769986027001077
10.1093/jxb/erv291
10.15252/embj.2020104763
10.1093/molbev/msv035
10.7554/eLife.23244
10.1002/0471250953.bi1112s47
10.1038/nature21034
10.1016/j.cell.2018.01.011
10.1534/g3.119.400201
10.1093/molbev/msm088
10.1371/journal.pgen.1008160
10.3390/ncrna6040041
10.1021/pr401280w
10.1073/pnas.1708433114
10.1007/978-1-4939-9045-0_25
10.1093/nar/gky1106
10.1038/nature05874
10.1016/j.tig.2017.05.004
10.1038/s41559-017-0146
10.1038/nrg3950
10.1126/science.1138341
10.1261/rna.053561.115
10.3389/fpls.2020.00276
10.1371/journal.pgen.1001115
10.1146/annurev-cellbio-100818-125218
10.1038/s41559-018-0506-6
10.1105/tpc.15.00440
10.1038/s41477-020-00769-x
10.1007/BF01731581
10.1093/molbev/msr263
10.1093/bioinformatics/18.12.1703
10.1038/nprot.2012.086
10.1093/nar/gkaa588
10.1186/s13059-017-1293-0
10.1007/s00239-020-09939-z
10.1016/j.yexcr.2020.112057
10.1038/nprot.2016.136
10.1093/bib/bby055
10.1038/nrm.2017.58
10.1093/nar/gkh340
10.1186/s12870-018-1611-z
10.1038/nrmicro3316
10.1093/bioinformatics/btp352
10.1128/MCB.00528-19
10.1038/nature14346
10.1111/2041-210X.13313
10.1038/s41467-020-15171-6
10.1016/j.cub.2018.05.068
10.1093/molbev/msx315
10.1186/s12859-014-0380-4
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References Zeng (2021100913442761900_B122) 2018; 19
Basile (2021100913442761900_B31) 2017; 13
Fesenko (2021100913442761900_B64) 2021; 22
Michel (2021100913442761900_B106) 2014; 15
Couso (2021100913442761900_B25) 2017; 18
Tang (2021100913442761900_B72) 2020; 11
Heames (2021100913442761900_B26) 2020; 88
Wissler (2021100913442761900_B128) 2012; 4
Ruiz-Orera (2021100913442761900_B94) 2018; 2
Bailey (2021100913442761900_B59) 1994; 2
Zhang (2021100913442761900_B108) 2015; 16
van Heesch (2021100913442761900_B17) 2019; 178
Shabalina (2021100913442761900_B118) 2014; 42
Ladoukakis (2021100913442761900_B89) 2011; 12
Hochberg (2021100913442761900_B124) 2020; 588
Martinez (2021100913442761900_B13) 2020; 16
Aspden (2021100913442761900_B112) 2014; 3
Hezroni (2021100913442761900_B130) 2017; 18
Perez-Riverol (2021100913442761900_B131) 2019; 47
Hao (2021100913442761900_B35) 2018; 19
Hazarika (2021100913442761900_B84) 2017; 18
Vakirlis (2021100913442761900_B27) 2020; 11
Brunet (2021100913442761900_B16) 2020; 393
Kavi Kishor (2021100913442761900_B113) 2015; 6
Hartford (2021100913442761900_B88) 2020; 40
Paytuvi-Gallart (2021100913442761900_B38) 2019; 1933
Kimura (2021100913442761900_B51) 1980; 16
Parker (2021100913442761900_B103) 2020; 9
Chaudhary (2021100913442761900_B91) 2017; 6
(2021100913442761900_B1) 2007; 447
Shabalina (2021100913442761900_B117) 2010; 27
Murrell (2021100913442761900_B53) 2015; 32
Gong (2021100913442761900_B14) 2011; 470
Altschul (2021100913442761900_B46) 1997; 25
Singh (2021100913442761900_B99) 2016; 6
Hezroni (2021100913442761900_B87) 2015; 11
Lex (2021100913442761900_B79) 2014; 20
Fesenko (2021100913442761900_B109) 2019; 19
Mergner (2021100913442761900_B85) 2020; 579
Resch (2021100913442761900_B93) 2009; 10
Sberro (2021100913442761900_B24) 2019; 178
Krogh (2021100913442761900_B62) 2001; 305
Eaton (2021100913442761900_B56) 2020; 11
Pearce (2021100913442761900_B114) 2011; 12
Miravet-Verde (2021100913442761900_B23) 2019; 15
Ingolia (2021100913442761900_B10) 2012; 7
Tyanova (2021100913442761900_B66) 2016; 11
Minati (2021100913442761900_B15) 2021; 10
Lauressergues (2021100913442761900_B120) 2015; 520
One Thousand Plant Transcriptomes Initiative (2021100913442761900_B45) 2019; 574
Ogurtsov (2021100913442761900_B47) 2002; 18
Armenteros (2021100913442761900_B61) 2019; 37
Li (2021100913442761900_B69) 2016; 32
Palazzo (2021100913442761900_B107) 2020; 183
Pauli (2021100913442761900_B5) 2012; 22
Dallagiovanna (2021100913442761900_B11) 2017; 610
Yu (2021100913442761900_B4) 2019; 35
Whitewoods (2021100913442761900_B101) 2018; 28
Ruiz Cuevas (2021100913442761900_B111) 2021; 34
Kopp (2021100913442761900_B6) 2018; 172
Sharma (2021100913442761900_B121) 2020; 6
Lang (2021100913442761900_B39) 2018; 93
Bazin (2021100913442761900_B8) 2017; 114
Huraiova (2021100913442761900_B20) 2020; 19
Kapranov (2021100913442761900_B2) 2007; 316
Vakirlis (2021100913442761900_B30) 2018; 35
Hershberg (2021100913442761900_B126) 2010; 6
Virtanen (2021100913442761900_B76) 2020; 17
Wade (2021100913442761900_B3) 2014; 12
Ulitsky (2021100913442761900_B81) 2016; 17
Colling (2021100913442761900_B100) 2015; 66
Olexiouk (2021100913442761900_B34) 2018; 46
Edgar (2021100913442761900_B48) 2004; 32
Budak (2021100913442761900_B80) 2020; 11
Rice (2021100913442761900_B42) 2000; 16
Suyama (2021100913442761900_B50) 2006; 34
Managadze (2021100913442761900_B92) 2013; 9
Szcześniak (2021100913442761900_B37) 2019; 1933
Yang (2021100913442761900_B52) 2007; 24
Jenuth (2021100913442761900_B44) 1999
Carvunis (2021100913442761900_B29) 2012; 487
Kirov (2021100913442761900_B105) 2020; 9
Wu (2021100913442761900_B123) 2020; 39
McKinney (2021100913442761900_B78) 2012
Kubo (2021100913442761900_B63) 2013; 8
Mackowiak (2021100913442761900_B90) 2015; 16
Toll-Riera (2021100913442761900_B95) 2012; 29
Choi (2021100913442761900_B86) 2019; 20
Zhang (2021100913442761900_B104) 2020; 48
Slavoff (2021100913442761900_B18) 2013; 9
Mortz (2021100913442761900_B116) 2020; 112
Wu (2021100913442761900_B7) 2017; 33
Fesenko (2021100913442761900_B22) 2019; 29
Wootton (2021100913442761900_B98) 1993; 17
Matsumoto (2021100913442761900_B125) 2017; 541
Wootton (2021100913442761900_B60) 1996
Li (2021100913442761900_B119) 2020; 9
Van Rossum (2021100913442761900_B75) 1995
Liao (2021100913442761900_B74) 2014; 30
Simopoulos (2021100913442761900_B40) 2019; 9
Kovaka (2021100913442761900_B71) 2019; 20
Bao (2021100913442761900_B115) 2017; 175
Ma (2021100913442761900_B19) 2014; 13
Quinlan (2021100913442761900_B41) 2014; 47
Waskom (2021100913442761900_B77) 2021; 6
Faurobert (2021100913442761900_B65) 2007; 355
Nesvizhskii (2021100913442761900_B67) 2014; 11
Zhu (2021100913442761900_B43) 2019; 20
Keeling (2021100913442761900_B129) 2019; 8
Ruiz-Orera (2021100913442761900_B36) 2019; 1
Kondrashov (2021100913442761900_B49) 2002; 11
Quevillon (2021100913442761900_B57) 2005; 33
Jarnot (2021100913442761900_B97) 2020
Chen (2021100913442761900_B110) 2020; 367
Gao (2021100913442761900_B83) 2015; 12
Dragomir (2021100913442761900_B32) 2020; 6
Tavormina (2021100913442761900_B102) 2015; 27
Li (2021100913442761900_B82) 2020; 30
Thissen (2021100913442761900_B55) 2002; 27
Nguyen (2021100913442761900_B54) 2015; 32
Ji (2021100913442761900_B12) 2015; 4
Ji (2021100913442761900_B33) 2020; 21
Wilson (2021100913442761900_B28) 2017; 1
Lang (2021100913442761900_B68) 2018; 93
Van Oss (2021100913442761900_B127) 2019; 15
Pertea (2021100913442761900_B73) 2020; 9
Wang (2021100913442761900_B21) 2020; 13
Boschiero (2021100913442761900_B58) 2019; 4
Radó-Trilla (2021100913442761900_B96) 2012; 12
Carlevaro-Fita (2021100913442761900_B9) 2016; 22
Li (2021100913442761900_B70) 2009; 25
References_xml – volume: 183
  start-page: 1151
  year: 2020
  ident: 2021100913442761900_B107
  article-title: Functional long non-coding RNAs evolve from junk transcripts
  publication-title: Cell
  doi: 10.1016/j.cell.2020.09.047
– volume: 4
  start-page: 441
  year: 2019
  ident: 2021100913442761900_B58
  article-title: Identification and functional investigation of genome-encoded, small, secreted peptides in plants
  publication-title: Curr. Protoc. Plant Biol.
  doi: 10.1002/cppb.20098
– volume: 305
  start-page: 567
  year: 2001
  ident: 2021100913442761900_B62
  article-title: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes
  publication-title: J. Mol. Biol.
  doi: 10.1006/jmbi.2000.4315
– volume: 33
  start-page: W116
  year: 2005
  ident: 2021100913442761900_B57
  article-title: InterProScan: protein domains identifier
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gki442
– volume: 15
  start-page: e8290
  year: 2019
  ident: 2021100913442761900_B23
  article-title: Unraveling the hidden universe of small proteins in bacterial genomes
  publication-title: Mol. Syst. Biol.
  doi: 10.15252/msb.20188290
– volume: 34
  start-page: W609
  year: 2006
  ident: 2021100913442761900_B50
  article-title: PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkl315
– volume: 470
  start-page: 284
  year: 2011
  ident: 2021100913442761900_B14
  article-title: lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements
  publication-title: Nature
  doi: 10.1038/nature09701
– volume: 32
  start-page: 2103
  year: 2016
  ident: 2021100913442761900_B69
  article-title: Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btw152
– volume: 4
  start-page: e7
  year: 2012
  ident: 2021100913442761900_B128
  article-title: Evolutionary dynamics of simple sequence repeats across long evolutionary time scale in genus Drosophila
  publication-title: Trends Evol. Biol.
  doi: 10.4081/eb.2012.e7
– volume: 16
  start-page: 179
  year: 2015
  ident: 2021100913442761900_B90
  article-title: Extensive identification and analysis of conserved small ORFs in animals
  publication-title: Genome Biol.
  doi: 10.1186/s13059-015-0742-x
– volume: 12
  start-page: R118
  year: 2011
  ident: 2021100913442761900_B89
  article-title: Hundreds of putatively functional small open reading frames in Drosophila
  publication-title: Genome Biol.
  doi: 10.1186/gb-2011-12-11-r118
– volume: 10
  start-page: e59303
  year: 2021
  ident: 2021100913442761900_B15
  article-title: One-shot analysis of translated mammalian lncRNAs with AHARIBO
  publication-title: Elife
  doi: 10.7554/eLife.59303
– volume: 112
  start-page: 1120
  year: 2020
  ident: 2021100913442761900_B116
  article-title: Comparative genomic analysis identifies small open reading frames (sORFs) with peptide-encoding features in avian 16S rDNA
  publication-title: Genomics
  doi: 10.1016/j.ygeno.2019.06.026
– volume: 10
  start-page: 162
  year: 2009
  ident: 2021100913442761900_B93
  article-title: Evolution of alternative and constitutive regions of mammalian 5′UTRs
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-10-162
– volume: 11
  start-page: 1114
  year: 2014
  ident: 2021100913442761900_B67
  article-title: Proteogenomics: concepts, applications and computational strategies
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.3144
– volume: 9
  start-page: 1794
  year: 2020
  ident: 2021100913442761900_B105
  article-title: Nanopore RNA sequencing revealed long non-coding and LTR retrotransposon-related RNAs expressed at early stages of triticale SEED development
  publication-title: Plants
  doi: 10.3390/plants9121794
– volume: 16
  start-page: 276
  year: 2000
  ident: 2021100913442761900_B42
  article-title: EMBOSS: the European Molecular Biology Open Software Suite
  publication-title: Trends Genet.
  doi: 10.1016/S0168-9525(00)02024-2
– volume: 175
  start-page: 619
  year: 2017
  ident: 2021100913442761900_B115
  article-title: Identification of novel growth regulators in plant populations expressing random peptides
  publication-title: Plant Physiol.
– volume: 8
  start-page: e47014
  year: 2019
  ident: 2021100913442761900_B129
  article-title: Philosophy of Biology: The meanings of’function’in biology and the problematic case of de novo gene emergence
  publication-title: Elife
  doi: 10.7554/eLife.47014
– volume: 9
  start-page: 59
  year: 2013
  ident: 2021100913442761900_B18
  article-title: Peptidomic discovery of short open reading frame-encoded peptides in human cells
  publication-title: Nat. Chem. Biol.
  doi: 10.1038/nchembio.1120
– volume: 18
  start-page: 37
  year: 2017
  ident: 2021100913442761900_B84
  article-title: ARA-PEPs: a repository of putative sORF-encoded peptides in Arabidopsis thaliana
  publication-title: BMC Bioinformatics
  doi: 10.1186/s12859-016-1458-y
– volume: 6
  start-page: 22352
  year: 2016
  ident: 2021100913442761900_B99
  article-title: Transmembrane domain lengths serve as signatures of organismal complexity and viral transport mechanisms
  publication-title: Sci. Rep.
  doi: 10.1038/srep22352
– volume: 1
  start-page: e2
  year: 2019
  ident: 2021100913442761900_B36
  article-title: Conserved regions in long non-coding RNAs contain abundant translation and protein–RNA interaction signatures
  publication-title: NAR Genom Bioinform
  doi: 10.1093/nargab/lqz002
– volume: 34
  start-page: 108815
  year: 2021
  ident: 2021100913442761900_B111
  article-title: Most non-canonical proteins uniquely populate the proteome or immunopeptidome
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2021.108815
– volume: 32
  start-page: 268
  year: 2015
  ident: 2021100913442761900_B54
  article-title: IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msu300
– volume: 19
  start-page: 636
  year: 2018
  ident: 2021100913442761900_B35
  article-title: SmProt: a database of small proteins encoded by annotated coding and non-coding RNA loci
  publication-title: Brief. Bioinform.
– volume: 17
  start-page: 149
  year: 1993
  ident: 2021100913442761900_B98
  article-title: Statistics of local complexity in amino acid sequences and sequence databases
  publication-title: Comput. Chem.
  doi: 10.1016/0097-8485(93)85006-X
– volume: 20
  start-page: 559
  year: 2019
  ident: 2021100913442761900_B43
  article-title: MiPepid: MicroPeptide identification tool using machine learning
  publication-title: BMC Bioinformatics
  doi: 10.1186/s12859-019-3033-9
– volume: 37
  start-page: 420
  year: 2019
  ident: 2021100913442761900_B61
  article-title: SignalP 5.0 improves signal peptide predictions using deep neural networks
  publication-title: Nat. Biotechnol.
  doi: 10.1038/s41587-019-0036-z
– volume: 11
  start-page: 781
  year: 2020
  ident: 2021100913442761900_B27
  article-title: De novo emergence of adaptive membrane proteins from thymine-rich genomic sequences
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-020-14500-z
– volume: 579
  start-page: 409
  year: 2020
  ident: 2021100913442761900_B85
  article-title: Mass-spectrometry-based draft of the Arabidopsis proteome
  publication-title: Nature
  doi: 10.1038/s41586-020-2094-2
– volume: 367
  start-page: 1140
  year: 2020
  ident: 2021100913442761900_B110
  article-title: Pervasive functional translation of noncanonical human open reading frames
  publication-title: Science
  doi: 10.1126/science.aay0262
– volume: 93
  start-page: 515
  year: 2018
  ident: 2021100913442761900_B39
  article-title: The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution
  publication-title: Plant J.
  doi: 10.1111/tpj.13801
– start-page: 169
  volume-title: Man-Machine Interactions 6
  year: 2020
  ident: 2021100913442761900_B97
  article-title: LCR-BLAST—a new modification of BLAST to search for similar low complexity regions in protein sequences
  doi: 10.1007/978-3-030-31964-9_16
– volume: 29
  start-page: 1464
  year: 2019
  ident: 2021100913442761900_B22
  article-title: Distinct types of short open reading frames are translated in plant cells
  publication-title: Genome Res.
  doi: 10.1101/gr.253302.119
– volume: 20
  start-page: 278
  year: 2019
  ident: 2021100913442761900_B71
  article-title: Transcriptome assembly from long-read RNA-seq alignments with StringTie2
  publication-title: Genome Biol.
  doi: 10.1186/s13059-019-1910-1
– volume: 3
  start-page: e03528
  year: 2014
  ident: 2021100913442761900_B112
  article-title: Extensive translation of small Open Reading Frames revealed by Poly-Ribo-Seq
  publication-title: Elife
  doi: 10.7554/eLife.03528
– volume: 9
  start-page: e53734
  year: 2020
  ident: 2021100913442761900_B119
  article-title: A small protein encoded by a putative lncRNA regulates apoptosis and tumorigenicity in human colorectal cancer cells
  publication-title: Elife
  doi: 10.7554/eLife.53734
– volume: 22
  start-page: 577
  year: 2012
  ident: 2021100913442761900_B5
  article-title: Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis
  publication-title: Genome Res.
  doi: 10.1101/gr.133009.111
– volume: 610
  start-page: 103
  year: 2017
  ident: 2021100913442761900_B11
  article-title: lncRNAs are associated with polysomes during adipose-derived stem cell differentiation
  publication-title: Gene
  doi: 10.1016/j.gene.2017.02.004
– volume: 19
  start-page: 1777
  year: 2020
  ident: 2021100913442761900_B20
  article-title: Proteomic analysis of meiosis and characterization of novel short open reading frames in the fission yeast Schizosaccharomyces pombe
  publication-title: Cell Cycle
  doi: 10.1080/15384101.2020.1779470
– volume: 11
  start-page: 669
  year: 2002
  ident: 2021100913442761900_B49
  article-title: Classification of common conserved sequences in mammalian intergenic regions
  publication-title: Hum. Mol. Genet.
  doi: 10.1093/hmg/11.6.669
– volume: 17
  start-page: 601
  year: 2016
  ident: 2021100913442761900_B81
  article-title: Evolution to the rescue: using comparative genomics to understand long non-coding RNAs
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg.2016.85
– volume: 178
  start-page: 1245
  year: 2019
  ident: 2021100913442761900_B24
  article-title: Large-scale analyses of human microbiomes reveal thousands of small, novel genes
  publication-title: Cell
  doi: 10.1016/j.cell.2019.07.016
– volume: 17
  start-page: 261
  year: 2020
  ident: 2021100913442761900_B76
  article-title: SciPy 1.0: fundamental algorithms for scientific computing in Python
  publication-title: Nat. Methods
  doi: 10.1038/s41592-019-0686-2
– volume: 2
  start-page: 28
  year: 1994
  ident: 2021100913442761900_B59
  article-title: Fitting a mixture model by expectation maximization to discover motifs in bipolymers
  publication-title: Proc. Int. Conf. Intell. Syst. Mol. Biol.
– volume: 25
  start-page: 3389
  year: 1997
  ident: 2021100913442761900_B46
  article-title: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
  publication-title: Nucleic. Acids. Res.
  doi: 10.1093/nar/25.17.3389
– volume: 20
  start-page: 1983
  year: 2014
  ident: 2021100913442761900_B79
  article-title: UpSet: visualization of intersecting sets
  publication-title: IEEE Trans. Vis. Comput. Graph.
  doi: 10.1109/TVCG.2014.2346248
– volume: 21
  start-page: 455
  year: 2020
  ident: 2021100913442761900_B33
  article-title: smORFunction: a tool for predicting functions of small open reading frames and microproteins
  publication-title: BMC Bioinformatics
  doi: 10.1186/s12859-020-03805-x
– volume: 1933
  start-page: 415
  year: 2019
  ident: 2021100913442761900_B37
  article-title: CANTATAdb 2.0: Expanding the Collection of Plant Long Noncoding RNAs
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-4939-9045-0_26
– volume: 13
  start-page: 1078
  year: 2020
  ident: 2021100913442761900_B21
  article-title: Large-scale discovery of non-conventional peptides in maize and Arabidopsis through an integrated peptidogenomic pipeline
  publication-title: Mol. Plant
  doi: 10.1016/j.molp.2020.05.012
– volume: 12
  start-page: 155
  year: 2012
  ident: 2021100913442761900_B96
  article-title: Dissecting the role of low-complexity regions in the evolution of vertebrate proteins
  publication-title: BMC Evol. Biol.
  doi: 10.1186/1471-2148-12-155
– volume: 9
  start-page: e49658
  year: 2020
  ident: 2021100913442761900_B103
  article-title: Nanopore direct RNA sequencing maps the complexity of Arabidopsis mRNA processing and m6A modification
  publication-title: Elife
  doi: 10.7554/eLife.49658
– volume: 19
  start-page: 414
  year: 2018
  ident: 2021100913442761900_B122
  article-title: Identification and analysis of ribosome-associated lncRNAs using ribosome profiling data
  publication-title: BMC Genomics
  doi: 10.1186/s12864-018-4765-z
– volume: 27
  start-page: 1745
  year: 2010
  ident: 2021100913442761900_B117
  article-title: Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msq086
– volume: 12
  start-page: 147
  year: 2015
  ident: 2021100913442761900_B83
  article-title: Quantitative profiling of initiating ribosomes in vivo
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.3208
– start-page: 554
  volume-title: Methods in Enzymology
  year: 1996
  ident: 2021100913442761900_B60
  article-title: [33]Analysis of compositionally biased regions in sequence databases
– volume: 4
  start-page: e08890
  year: 2015
  ident: 2021100913442761900_B12
  article-title: Many lncRNAs, 5′UTRs, and pseudogenes are translated and some are likely to express functional proteins
  publication-title: Elife
  doi: 10.7554/eLife.08890
– volume: 9
  start-page: 304
  year: 2020
  ident: 2021100913442761900_B73
  article-title: GFF utilities: GffRead and GffCompare
  publication-title: F1000Res
  doi: 10.12688/f1000research.23297.1
– volume: 30
  start-page: 1418
  year: 2020
  ident: 2021100913442761900_B82
  article-title: Prevalence of alternative AUG and non-AUG translation initiators and their regulatory effects across plants
  publication-title: Genome Res.
  doi: 10.1101/gr.261834.120
– volume: 6
  start-page: 3021
  year: 2021
  ident: 2021100913442761900_B77
  article-title: seaborn: statistical data visualization
  publication-title: J. Open Source Softw.
  doi: 10.21105/joss.03021
– volume: 487
  start-page: 370
  year: 2012
  ident: 2021100913442761900_B29
  article-title: Proto-genes and de novo gene birth
  publication-title: Nature
  doi: 10.1038/nature11184
– start-page: 301
  volume-title: Bioinformatics Methods and Protocols
  year: 1999
  ident: 2021100913442761900_B44
  article-title: The NCBI
  doi: 10.1385/1-59259-192-2:301
– volume: 30
  start-page: 923
  year: 2014
  ident: 2021100913442761900_B74
  article-title: featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btt656
– volume: 8
  start-page: e77356
  year: 2013
  ident: 2021100913442761900_B63
  article-title: System for stable β-estradiol-inducible gene expression in the moss Physcomitrella patens
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0077356
– volume: 11
  start-page: 1110
  year: 2015
  ident: 2021100913442761900_B87
  article-title: Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2015.04.023
– volume: 588
  start-page: 503
  year: 2020
  ident: 2021100913442761900_B124
  article-title: A hydrophobic ratchet entrenches molecular complexes
  publication-title: Nature
  doi: 10.1038/s41586-020-3021-2
– volume: 12
  start-page: 399
  year: 2011
  ident: 2021100913442761900_B114
  article-title: Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors
  publication-title: Curr. Protein Pept. Sci.
  doi: 10.2174/138920311796391106
– volume: 16
  start-page: 458
  year: 2020
  ident: 2021100913442761900_B13
  article-title: Accurate annotation of human protein-coding small open reading frames
  publication-title: Nat. Chem. Biol.
  doi: 10.1038/s41589-019-0425-0
– volume: 9
  start-page: e1002917
  year: 2013
  ident: 2021100913442761900_B92
  article-title: The vast, conserved mammalian lincRNome
  publication-title: PLoS Comput. Biol.
  doi: 10.1371/journal.pcbi.1002917
– volume: 42
  start-page: 7132
  year: 2014
  ident: 2021100913442761900_B118
  article-title: Evolution at protein ends: major contribution of alternative transcription initiation and termination to the transcriptome and proteome diversity in mammals
  publication-title: Nucleic. Acids. Res.
  doi: 10.1093/nar/gku342
– volume: 574
  start-page: 679
  year: 2019
  ident: 2021100913442761900_B45
  article-title: One thousand plant transcriptomes and the phylogenomics of green plants
  publication-title: Nature
  doi: 10.1038/s41586-019-1693-2
– volume: 178
  start-page: 242
  year: 2019
  ident: 2021100913442761900_B17
  article-title: The translational landscape of the human heart
  publication-title: Cell
  doi: 10.1016/j.cell.2019.05.010
– volume: 46
  start-page: D497
  year: 2018
  ident: 2021100913442761900_B34
  article-title: An update on sORFs.org: a repository of small ORFs identified by ribosome profiling
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx1130
– volume: 22
  start-page: 77
  year: 2021
  ident: 2021100913442761900_B64
  article-title: Role of the methionine cycle in the temperature-sensitive responses of potato plants to potato virus Y
  publication-title: Mol. Plant Pathol.
  doi: 10.1111/mpp.13009
– volume: 13
  start-page: e1005375
  year: 2017
  ident: 2021100913442761900_B31
  article-title: High GC content causes orphan proteins to be intrinsically disordered
  publication-title: PLoS Comput. Biol.
  doi: 10.1371/journal.pcbi.1005375
– volume: 27
  start-page: 77
  year: 2002
  ident: 2021100913442761900_B55
  article-title: Quick and easy implementation of the Benjamini-Hochberg procedure for controlling the false positive rate in multiple comparisons
  publication-title: J. Educ. Behav. Stat.
  doi: 10.3102/10769986027001077
– volume: 355
  start-page: 9
  year: 2007
  ident: 2021100913442761900_B65
  article-title: Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues
  publication-title: Methods Mol. Biol.
– volume: 66
  start-page: 5337
  year: 2015
  ident: 2021100913442761900_B100
  article-title: Overexpression of the Arabidopsis thaliana signalling peptide TAXIMIN1 affects lateral organ development
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/erv291
– year: 2012
  ident: 2021100913442761900_B78
– volume: 39
  start-page: e104763
  year: 2020
  ident: 2021100913442761900_B123
  article-title: Translation of small downstream ORFs enhances translation of canonical main open reading frames
  publication-title: EMBO J.
  doi: 10.15252/embj.2020104763
– volume: 32
  start-page: 1365
  year: 2015
  ident: 2021100913442761900_B53
  article-title: Gene-wide identification of episodic selection
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msv035
– volume: 6
  start-page: e23244
  year: 2017
  ident: 2021100913442761900_B91
  article-title: Prosurvival long noncoding RNA PINCR regulates a subset of p53 targets in human colorectal cancer cells by binding to Matrin 3
  publication-title: Elife
  doi: 10.7554/eLife.23244
– volume: 47
  start-page: 11
  year: 2014
  ident: 2021100913442761900_B41
  article-title: BEDTools: the Swiss-army tool for genome feature analysis
  publication-title: Curr. Protoc. Bioinformatics
  doi: 10.1002/0471250953.bi1112s47
– volume: 541
  start-page: 228
  year: 2017
  ident: 2021100913442761900_B125
  article-title: mTORC1 and muscle regeneration are regulated by the LINC00961-encoded SPAR polypeptide
  publication-title: Nature
  doi: 10.1038/nature21034
– volume: 172
  start-page: 393
  year: 2018
  ident: 2021100913442761900_B6
  article-title: Functional classification and experimental dissection of long noncoding RNAs
  publication-title: Cell
  doi: 10.1016/j.cell.2018.01.011
– volume: 9
  start-page: 2511
  year: 2019
  ident: 2021100913442761900_B40
  article-title: Molecular traits of long non-protein coding RNAs from diverse plant species show little evidence of phylogenetic relationships
  publication-title: G3
  doi: 10.1534/g3.119.400201
– year: 1995
  ident: 2021100913442761900_B75
– volume: 24
  start-page: 1586
  year: 2007
  ident: 2021100913442761900_B52
  article-title: PAML 4: phylogenetic analysis by maximum likelihood
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msm088
– volume: 15
  start-page: e1008160
  year: 2019
  ident: 2021100913442761900_B127
  article-title: De novo gene birth
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1008160
– volume: 6
  start-page: 41
  year: 2020
  ident: 2021100913442761900_B32
  article-title: FuncPEP: a database of functional peptides encoded by non-coding RNAs
  publication-title: Noncoding RNA
  doi: 10.3390/ncrna6040041
– volume: 13
  start-page: 1757
  year: 2014
  ident: 2021100913442761900_B19
  article-title: Discovery of human sORF-encoded polypeptides (SEPs) in cell lines and tissue
  publication-title: J. Proteome Res.
  doi: 10.1021/pr401280w
– volume: 114
  start-page: E10018
  year: 2017
  ident: 2021100913442761900_B8
  article-title: Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1708433114
– volume: 1933
  start-page: 397
  year: 2019
  ident: 2021100913442761900_B38
  article-title: A walkthrough to the use of GreeNC: the plant lncRNA database
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-4939-9045-0_25
– volume: 47
  start-page: D442
  year: 2019
  ident: 2021100913442761900_B131
  article-title: The PRIDE database and related tools and resources in 2019: improving support for quantification data
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky1106
– volume: 447
  start-page: 799
  year: 2007
  ident: 2021100913442761900_B1
  article-title: Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project
  publication-title: Nature
  doi: 10.1038/nature05874
– volume: 33
  start-page: 540
  year: 2017
  ident: 2021100913442761900_B7
  article-title: The diversity of long noncoding RNAs and their generation
  publication-title: Trends Genet.
  doi: 10.1016/j.tig.2017.05.004
– volume: 1
  start-page: 0146
  year: 2017
  ident: 2021100913442761900_B28
  article-title: Young genes are highly disordered as predicted by the preadaptation hypothesis of de novo gene birth
  publication-title: Nat. Ecol. Evol.
  doi: 10.1038/s41559-017-0146
– volume: 16
  start-page: 409
  year: 2015
  ident: 2021100913442761900_B108
  article-title: Determinants of the rate of protein sequence evolution
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg3950
– volume: 316
  start-page: 1484
  year: 2007
  ident: 2021100913442761900_B2
  article-title: RNA maps reveal new RNA classes and a possible function for pervasive transcription
  publication-title: Science
  doi: 10.1126/science.1138341
– volume: 22
  start-page: 867
  year: 2016
  ident: 2021100913442761900_B9
  article-title: Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
  publication-title: RNA
  doi: 10.1261/rna.053561.115
– volume: 11
  start-page: 276
  year: 2020
  ident: 2021100913442761900_B80
  article-title: Long non-coding RNA in plants in the era of reference sequences
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2020.00276
– volume: 6
  start-page: e1001115
  year: 2010
  ident: 2021100913442761900_B126
  article-title: Evidence that mutation is universally biased towards AT in bacteria
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1001115
– volume: 35
  start-page: 407
  year: 2019
  ident: 2021100913442761900_B4
  article-title: Plant Noncoding RNAs: hidden players in development and stress responses
  publication-title: Annu. Rev. Cell Dev. Biol.
  doi: 10.1146/annurev-cellbio-100818-125218
– volume: 2
  start-page: 890
  year: 2018
  ident: 2021100913442761900_B94
  article-title: Translation of neutrally evolving peptides provides a basis for de novo gene evolution
  publication-title: Nat. Ecol. Evol.
  doi: 10.1038/s41559-018-0506-6
– volume: 27
  start-page: 2095
  year: 2015
  ident: 2021100913442761900_B102
  article-title: The plant peptidome: an expanding repertoire of structural features and biological functions
  publication-title: Plant Cell
  doi: 10.1105/tpc.15.00440
– volume: 6
  start-page: 1262
  year: 2020
  ident: 2021100913442761900_B121
  article-title: Primary transcript of miR858 encodes regulatory peptide and controls flavonoid biosynthesis and development in Arabidopsis
  publication-title: Nat. Plants
  doi: 10.1038/s41477-020-00769-x
– volume: 16
  start-page: 111
  year: 1980
  ident: 2021100913442761900_B51
  article-title: A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences
  publication-title: J. Mol. Evol.
  doi: 10.1007/BF01731581
– volume: 29
  start-page: 883
  year: 2012
  ident: 2021100913442761900_B95
  article-title: Role of low-complexity sequences in the formation of novel protein coding sequences
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msr263
– volume: 6
  start-page: 544
  year: 2015
  ident: 2021100913442761900_B113
  article-title: Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny
  publication-title: Front. Plant Sci.
– volume: 18
  start-page: 1703
  year: 2002
  ident: 2021100913442761900_B47
  article-title: OWEN: aligning long collinear regions of genomes
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/18.12.1703
– volume: 7
  start-page: 1534
  year: 2012
  ident: 2021100913442761900_B10
  article-title: The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2012.086
– volume: 48
  start-page: 7700
  year: 2020
  ident: 2021100913442761900_B104
  article-title: New insights into Arabidopsis transcriptome complexity revealed by direct sequencing of native RNAs
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkaa588
– volume: 18
  start-page: 162
  year: 2017
  ident: 2021100913442761900_B130
  article-title: A subset of conserved mammalian long non-coding RNAs are fossils of ancestral protein-coding genes
  publication-title: Genome Biol.
  doi: 10.1186/s13059-017-1293-0
– volume: 88
  start-page: 382
  year: 2020
  ident: 2021100913442761900_B26
  article-title: A continuum of evolving de novo genes drives protein-coding novelty in Drosophila
  publication-title: J. Mol. Evol.
  doi: 10.1007/s00239-020-09939-z
– volume: 393
  start-page: 112057
  year: 2020
  ident: 2021100913442761900_B16
  article-title: Reconsidering proteomic diversity with functional investigation of small ORFs and alternative ORFs
  publication-title: Exp. Cell Res.
  doi: 10.1016/j.yexcr.2020.112057
– volume: 11
  start-page: 2301
  year: 2016
  ident: 2021100913442761900_B66
  article-title: The MaxQuant computational platform for mass spectrometry-based shotgun proteomics
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2016.136
– volume: 20
  start-page: 1853
  year: 2019
  ident: 2021100913442761900_B86
  article-title: The small peptide world in long noncoding RNAs
  publication-title: Brief. Bioinform.
  doi: 10.1093/bib/bby055
– volume: 18
  start-page: 575
  year: 2017
  ident: 2021100913442761900_B25
  article-title: Classification and function of small open reading frames
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/nrm.2017.58
– volume: 32
  start-page: 1792
  year: 2004
  ident: 2021100913442761900_B48
  article-title: MUSCLE: multiple sequence alignment with high accuracy and high throughput
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkh340
– volume: 19
  start-page: 9
  year: 2019
  ident: 2021100913442761900_B109
  article-title: Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the moss Physcomitrella patens
  publication-title: BMC Plant Biol.
  doi: 10.1186/s12870-018-1611-z
– volume: 12
  start-page: 647
  year: 2014
  ident: 2021100913442761900_B3
  article-title: Pervasive transcription: illuminating the dark matter of bacterial transcriptomes
  publication-title: Nat. Rev. Microbiol.
  doi: 10.1038/nrmicro3316
– volume: 25
  start-page: 2078
  year: 2009
  ident: 2021100913442761900_B70
  article-title: The Sequence Alignment/Map format and SAMtools
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp352
– volume: 93
  start-page: 515
  year: 2018
  ident: 2021100913442761900_B68
  article-title: The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution
  publication-title: Plant J.
  doi: 10.1111/tpj.13801
– volume: 40
  start-page: e00528-19
  year: 2020
  ident: 2021100913442761900_B88
  article-title: When long noncoding becomes protein coding
  publication-title: Mol. Cell. Biol.
  doi: 10.1128/MCB.00528-19
– volume: 520
  start-page: 90
  year: 2015
  ident: 2021100913442761900_B120
  article-title: Primary transcripts of microRNAs encode regulatory peptides
  publication-title: Nature
  doi: 10.1038/nature14346
– volume: 11
  start-page: 187
  year: 2020
  ident: 2021100913442761900_B56
  article-title: Toytree: a minimalist tree visualization and manipulation library for Python
  publication-title: Methods Ecol. Evol.
  doi: 10.1111/2041-210X.13313
– volume: 11
  start-page: 1438
  year: 2020
  ident: 2021100913442761900_B72
  article-title: Full-length transcript characterization of SF3B1 mutation in chronic lymphocytic leukemia reveals downregulation of retained introns
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-020-15171-6
– volume: 28
  start-page: 2365
  year: 2018
  ident: 2021100913442761900_B101
  article-title: CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants
  publication-title: Curr. Biol.
  doi: 10.1016/j.cub.2018.05.068
– volume: 35
  start-page: 631
  year: 2018
  ident: 2021100913442761900_B30
  article-title: A molecular portrait of de novo genes in yeasts
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msx315
– volume: 15
  start-page: 380
  year: 2014
  ident: 2021100913442761900_B106
  article-title: Computational approach for calculating the probability of eukaryotic translation initiation from ribo-seq data that takes into account leaky scanning
  publication-title: BMC Bioinformatics
  doi: 10.1186/s12859-014-0380-4
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Snippet Pervasive transcription of eukaryotic genomes results in expression of long non-coding RNAs (lncRNAs) most of which are poorly conserved in evolution and...
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SubjectTerms Bryopsida - genetics
Computational Biology
Open Reading Frames
Proteome
RNA, Long Noncoding
Transcriptome
Title A vast pool of lineage-specific microproteins encoded by long non-coding RNAs in plants
URI https://www.ncbi.nlm.nih.gov/pubmed/34570232
https://www.proquest.com/docview/2576915583
https://pubmed.ncbi.nlm.nih.gov/PMC8501992
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