Genome-wide identification and characterization of tRNA-derived RNA fragments in land plants.
The manuscript by Alves et al. entitled "Genome-wide identification and characterization of tRNA-derived RNA fragments in land plants" describes the identification and characterization of tRNAderived sRNA fragments in plants. By combining bioinformatic analysis and genetic and molecular approaches, we show that tRF biogenesis does not rely on canonical microRNA/siRNA processing machinery (i.e., independent of DICER-LIKE proteins). Moreover, we provide evidences that the Arabidopsis S-like Ribonuclease 1 (RNS1) might be involved in the biogenesis of tRFs. Detailed analyses showed that plant tRFs are sorted into different types of ARGONAUTE proteins and that they have potential target candidate genes. Our work advances the understanding of the tRF biology in plants by providing evidences that plant and animal tRFs shared common features and raising the hypothesis that an interplay between tRFs and other sRNAs might be important to fine-tune gene expression and protein biosynthesis in plant cells. Small RNA (sRNA) fragments derived from tRNAs (3'-loop, 5'-loop, anti-codon loop), named tRFs, have been reported in several organisms, including humans and plants. Although they may interfere with gene expression, their biogenesis and biological functions in plants remain poorly understood. Here, we capitalized on small RNA sequencing data from distinct species such as Arabidopsis thaliana, Oryza sativa, and Physcomitrella patens to examine the diversity of plant tRFs and provide insight into their properties. In silico analyzes of 19 to 25-nt tRFs derived from 5' (tRF-5s) and 3'CCA (tRF-3s) tRNA loops in these three evolutionary distant species showed that they are conserved and their abundance did not correlate with the number of genomic copies of the parental tRNAs. Moreover, tRF-5 is the most abundant variant in all three species. In silico and in vivo expression analyses unraveled differential accumulation of tRFs in Arabidopsis tissues/organs, suggesting that they are not byproducts of tRNA degradation. We also verified that the biogenesis of most Arabidopsis 19-25 nt tRF-5s and tRF-3s is not primarily dependent on DICER-LIKE proteins, though they seem to be associated with ARGONAUTE proteins and have few potential targets. Finally, we provide evidence that Arabidopsis ribonuclease RNS1 might be involved in the processing and/or degradation of tRFs. Our data support the notion that an interplay between tRFs and other sRNAs might be important to fine tune gene expression and protein biosynthesis in plant cells.
Departamento de Genetica, Instituto de Biociencias, Universidade Estadual Paulista (UNESP), Distrito de Rubião Jr., s/n, Botucatu, SP, 18618-970, Brazil.|Laboratorio de Genetica Molecular do Desenvolvimento Vegetal, Departamento de Ciencias Biologicas, ESALQ/USP, Avenida Pádua Dias s/n, 11, Piracicaba, SP, 13418-900, Brazil.
Cristiane S
CS
Alves
Laboratorio de Bioinformatica e Biologia de Sistemas, Departamento de Genetica, Evoluçao e Bioagentes, Universidade Estadual de Campinas (Unicamp), Campinas, SP, Brazil.
Renato
R
Vicentini
Centro de Biologia Molecular e Engenharia Genetica (CBMEG), Universidade Estadual de Campinas (Unicamp), Campinas, SP, Brazil.
Gustavo T
GT
Duarte
Departamento de Genetica, Instituto de Biociencias, Universidade Estadual Paulista (UNESP), Distrito de Rubião Jr., s/n, Botucatu, SP, 18618-970, Brazil.
Vitor F
VF
Pinoti
Centro de Biologia Molecular e Engenharia Genetica (CBMEG), Universidade Estadual de Campinas (Unicamp), Campinas, SP, Brazil.
Michel
M
Vincentz
Laboratorio de Genetica Molecular do Desenvolvimento Vegetal, Departamento de Ciencias Biologicas, ESALQ/USP, Avenida Pádua Dias s/n, 11, Piracicaba, SP, 13418-900, Brazil. ftsnogue@usp.br.
Fabio T S
http://orcid.org/0000-0001-6613-4069
FT
Nogueira
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D019068:Bryopsida / Q000235:genetics / Q000378:metabolism; D019295:Computational Biology; D018745:Genome, Plant; D012275:Oryza / Q000235:genetics / Q000378:metabolism; D018384:Oxidative Stress; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D018749:RNA, Plant / Q000737:chemistry* / Q000378:metabolism; D012343:RNA, Transfer / Q000737:chemistry* / Q000378:metabolism; D060888:Real-Time Polymerase Chain Reaction; D012260:Ribonucleases / Q000235:genetics / Q000378:metabolism / Q000502:physiology
D010940:Plant Proteins; D018749:RNA, Plant; D012343:RNA, Transfer; D012260:Ribonucleases; C489908:S-like RNase protein, plant
Arabidopsis thaliana; High throughput data; Small RNA; tRF; tRNA-derived RNA fragment
Plant Methods. 2007 Oct 12;3:12
17931426
Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):9970-5
18632569
RNA Biol. 2013 Apr;10(4):553-63
23563448
RNA Biol. 2011 May-Jun;8(3):538-47
21525786
Plant Cell. 2006 Nov;18(11):2985-98
17138694
Nucleic Acids Res. 2009 Oct;37(19):6575-86
19729508
Biol Direct. 2013 Feb 12;8:6
23402430
Mol Cell. 2010 Mar 12;37(5):668-78
20227371
Nat Struct Mol Biol. 2008 Oct;15(10):1015-23
18776903
Development. 2010 Nov;137(21):3535-43
20940223
Trends Genet. 2011 Oct;27(10):422-32
21741109
Methods. 2001 Dec;25(4):402-8
11846609
BMC Microbiol. 2014 Dec 10;14:308
25492044
Mol Genet Genomics. 2010 Apr;283(4):381-96
20182746
RNA. 2008 Oct;14(10):2095-103
18719243
J Exp Bot. 2013 Nov;64(14):4301-12
23997203
Mol Biol Evol. 2011 Oct;28(10):2731-9
21546353
Front Genet. 2014 Jun 11;5:171
24966867
Mol Cell. 2011 Aug 19;43(4):613-23
21855800
Nucleic Acids Res. 2012 Aug;40(14):6787-99
22492706
J Exp Bot. 2013 May;64(8):2307-20
23564956
RNA Biol. 2010 Mar-Apr;7(2):237-47
20224293
Plant Cell Environ. 2006 Mar;29(3):426-34
17080596
Plant J. 1994 Nov;6(5):673-85
8000425
RNA Biol. 2013 Dec;10 (12 ):1798-806
24351723
Mol Cell. 2016 Jan 21;61(2):222-35
26711010
J Biol Chem. 2010 Apr 2;285(14):10959-68
20129916
Plant Physiol. 2009 Dec;151(4):2120-32
19854858
Science. 2003 Apr 11;300(5617):332-6
12690200
Oncotarget. 2016 Apr 26;7(17):24766-77
27015120
RNA. 2010 Apr;16(4):673-95
20181738
PLoS Biol. 2004 May;2(5):E104
15024409
Trends Cell Biol. 2008 Mar;18(3):98-104
18262788
Nucleic Acids Res. 2011 Jul;39(Web Server issue):W155-9
21622958
BMC Mol Biol. 2015 Dec 22;16:22
26694924
Sci Rep. 2016 Feb 11;6:20850
26865164
Mol Genet Genomics. 2008 Sep;280(3):249-61
18607631
BMC Biol. 2014 Oct 01;12:78
25270025
DNA Res. 2013 Apr;20(2):109-25
23266877
Curr Biol. 2004 Feb 17;14(4):346-51
14972688
Archaea. 2012;2012:260909
23326205
J Cell Biol. 2009 Apr 6;185(1):35-42
19332886
Development. 2008 Apr;135(7):1201-14
18287206
J Plant Physiol. 2009 Dec 15;166(18):1982-92
19709775
RNA Biol. 2015;12(5):501-8
25833336
PLoS Genet. 2008 Feb;4(2):e27
18266474
RNA. 2009 Dec;15(12):2147-60
19850906
PLoS One. 2011;6(8):e23776
21912606
Nat Commun. 2014;5:3064
24451981
Genes Dev. 2009 Nov 15;23(22):2639-49
19933153
Nucleic Acids Res. 2009 Jan;37(Database issue):D93-7
18984615
Nucleic Acids Res. 2013 Jan;41(Database issue):D991-5
23193258
Genomics Inform. 2015 Dec;13(4):94-101
26865839
Cold Spring Harb Symp Quant Biol. 2006;71:157-64
17381292
Curr Opin Struct Biol. 2006 Feb;16(1):12-7
16364630
Genes Dev. 2010 Sep 1;24(17):1832-60
20810645
Biochim Biophys Acta. 2014 Dec;1839(12):1362-72
24560929
Nat Genet. 2006 Jun;38(6):721-5
16699516
Plant Cell Environ. 2008 Apr;31(4):562-74
18208512
Cell. 2008 Apr 4;133(1):116-27
18342361
Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12984-9
16129836
Nat Biotechnol. 2008 Aug;26(8):941-6
18542052
Mol Cell. 2013 Sep 12;51(5):594-605
24034694
RNA Biol. 2013 Dec;10(12):1853-67
24448271
PLoS One. 2013 May 14;8(5):e64003
23691136
Front Plant Sci. 2016 Jun 01;7:767
27313593