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PMID: 28335016 Published · ppublish English Journal Article

tRNA-derived small RNAs target transposable element transcripts.

Nucleic acids research ·Vol. 45 ·No. 9 ·2017-05-19 ·Pages 5142-5152

Martinez G, Choudury SG, Slotkin RK

Abstract

tRNA-derived RNA fragments (tRFs) are 18-26 nucleotide small RNAs that are not random degradation products, but are rather specifically cleaved from mature tRNA transcripts. Abundant in stressed or viral-infected cells, the function and potential targets of tRFs are not known. We identified that in the unstressed wild-type male gamete containing pollen of flowering plants, and analogous reproductive structure in non-flowering plant species, tRFs accumulate to high levels. In the reference plant Arabidopsis thaliana, tRFs are processed by Dicer-like 1 and incorporated into Argonaute1 (AGO1), akin to a microRNA. We utilized the fact that many plant small RNAs direct cleavage of their target transcripts to demonstrate that the tRF-AGO1 complex acts to specifically target and cleave endogenous transposable element (TE) mRNAs produced from transcriptionally active TEs. The data presented here demonstrate that tRFs are bona-fide regulatory microRNA-like small RNAs involved in the regulation of genome stability through the targeting of TE transcripts.

MeSH Terms
Arabidopsis/genetics Arabidopsis Proteins/metabolism Base Sequence DNA Transposable Elements/genetics MicroRNAs/metabolism Mutation/genetics Pollen/metabolism RNA, Messenger/genetics,metabolism RNA, Plant/genetics,metabolism RNA, Transfer/genetics,metabolism Reproducibility of Results
Chemicals
Arabidopsis Proteins DNA Transposable Elements MicroRNAs RNA, Messenger RNA, Plant RNA, Transfer
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Martinez German
Department of Molecular Genetics and Center for RNA Biology, The Ohio State University, Columbus, 43210 OH, USA. | Department of Plant Biology, Swedish University of Agricultural Sciences and Linnean Center of Plant Biology, 75007 Uppsala, Sweden.
Choudury Sarah G
Department of Molecular Genetics and Center for RNA Biology, The Ohio State University, Columbus, 43210 OH, USA. | Molecular, Cellular and Developmental Biology Graduate Program, The Ohio State University, Columbus, 43210 OH, USA. | Center for RNA Biology, The Ohio State University, Columbus, 43210 OH, USA.
Slotkin R Keith
Department of Molecular Genetics and Center for RNA Biology, The Ohio State University, Columbus, 43210 OH, USA. | Center for RNA Biology, The Ohio State University, Columbus, 43210 OH, USA.
References (48)
48 references, click to expand
  1. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA.
    PLoS Genet. 2012 Feb;8(2):e1002474 PMID: 22346759
  2. The Lupus Autoantigen La Prevents Mis-channeling of tRNA Fragments into the Human MicroRNA Pathway.
    Mol Cell. 2016 Jul 7;63(1):110-24 PMID: 27345152
  3. Hints of tRNA-Derived Small RNAs Role in RNA Silencing Mechanisms.
    Genes (Basel). 2012 Oct 10;3(4):603-14 PMID: 24705078
  4. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin.
    EMBO Rep. 2009 Sep;10(9):1015-21 PMID: 19680290
  5. Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell.
    Nat Plants. 2016 Mar 21;2:16030 PMID: 27249563
  6. Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid.
    Nucleic Acids Res. 2009 Oct;37(19):6575-86 PMID: 19729508
  7. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals.
    Science. 2016 Jan 22;351(6271):391-396 PMID: 26721685
  8. Developmental relaxation of transposable element silencing in plants: functional or byproduct?
    Curr Opin Plant Biol. 2012 Nov;15(5):496-502 PMID: 23022393
  9. Description of plant tRNA-derived RNA fragments (tRFs) associated with argonaute and identification of their putative targets.
    Biol Direct. 2013 Feb 12;8:6 PMID: 23402430
  10. 5' tRNA Halves: The Next Generation of Immune Signaling Molecules.
    Front Immunol. 2015 Feb 19;6:74 PMID: 25745425
  11. Angiogenin-induced tRNA fragments inhibit translation initiation.
    Mol Cell. 2011 Aug 19;43(4):613-23 PMID: 21855800
  12. Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs.
    Nucleic Acids Res. 2012 Aug;40(14):6787-99 PMID: 22492706
  13. miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis.
    Nature. 2014 Apr 17;508(7496):411-5 PMID: 24670663
  14. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.
    Cell. 2013 Mar 28;153(1):193-205 PMID: 23540698
  15. The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation.
    Plant Physiol. 2009 May;150(1):378-87 PMID: 19261735
  16. Regulatory RNAs derived from transfer RNA?
    RNA. 2010 Oct;16(10):1865-9 PMID: 20719919
  17. A highly specific microRNA-mediated mechanism silences LTR retrotransposons of strawberry.
    Plant J. 2016 Jan;85(1):70-82 PMID: 26611654
  18. Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis.
    Plant Cell. 2012 Feb;24(2):415-27 PMID: 22345490
  19. Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin.
    RNA Biol. 2011 Jan-Feb;8(1):158-77 PMID: 21282978
  20. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing.
    Plant Physiol. 2009 Dec;151(4):2120-32 PMID: 19854858
  21. tRNA processing defects induce replication stress and Chk2-dependent disruption of piRNA transcription.
    EMBO J. 2015 Dec 14;34(24):3009-27 PMID: 26471728
  22. A dual program for translation regulation in cellular proliferation and differentiation.
    Cell. 2014 Sep 11;158(6):1281-1292 PMID: 25215487
  23. MicroRNAS and their regulatory roles in plants.
    Annu Rev Plant Biol. 2006;57:19-53 PMID: 16669754
  24. Human tRNA-derived small RNAs in the global regulation of RNA silencing.
    RNA. 2010 Apr;16(4):673-95 PMID: 20181738
  25. The moss Physcomitrella patens, now and then.
    Plant Physiol. 2001 Dec;127(4):1430-8 PMID: 11743086
  26. psRNATarget: a plant small RNA target analysis server.
    Nucleic Acids Res. 2011 Jul;39(Web Server issue):W155-9 PMID: 21622958
  27. A human snoRNA with microRNA-like functions.
    Mol Cell. 2008 Nov 21;32(4):519-28 PMID: 19026782
  28. Transposable elements and the epigenetic regulation of the genome.
    Nat Rev Genet. 2007 Apr;8(4):272-85 PMID: 17363976
  29. Genome-wide identification of genes regulated in trans by transposable element small interfering RNAs.
    RNA Biol. 2013 Aug;10(8):1379-95 PMID: 23863322
  30. Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets.
    BMC Biol. 2014 Oct 01;12:78 PMID: 25270025
  31. A comprehensive expression profile of microRNAs and other classes of non-coding small RNAs in barley under phosphorous-deficient and -sufficient conditions.
    DNA Res. 2013 Apr;20(2):109-25 PMID: 23266877
  32. tRNA-derived fragments target the ribosome and function as regulatory non-coding RNA in Haloferax volcanii.
    Archaea. 2012;2012:260909 PMID: 23326205
  33. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs.
    RNA. 2009 Dec;15(12):2147-60 PMID: 19850906
  34. Beyond microRNA--novel RNAs derived from small non-coding RNA and their implication in cancer.
    Cancer Lett. 2013 Nov 1;340(2):201-11 PMID: 23376637
  35. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen.
    Cell. 2009 Feb 6;136(3):461-72 PMID: 19203581
  36. Transposable element origins of epigenetic gene regulation.
    Curr Opin Plant Biol. 2011 Apr;14(2):156-61 PMID: 21444239
  37. The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets.
    Bioinformatics. 2012 Aug 1;28(15):2059-61 PMID: 22628521
  38. Hidden layers of human small RNAs.
    BMC Genomics. 2008 Apr 10;9:157 PMID: 18402656
  39. RNA silencing in plants.
    Nature. 2004 Sep 16;431(7006):356-63 PMID: 15372043
  40. MicroRNA activity in the Arabidopsis male germline.
    J Exp Bot. 2011 Mar;62(5):1611-20 PMID: 21357774
  41. Genome-wide identification and characterization of tRNA-derived RNA fragments in land plants.
    Plant Mol Biol. 2017 Jan;93(1-2):35-48 PMID: 27681945
  42. An expression atlas of rice mRNAs and small RNAs.
    Nat Biotechnol. 2007 Apr;25(4):473-7 PMID: 17351617
  43. tRNAs: new tricks from old dogs.
    EMBO J. 2014 Sep 17;33(18):1981-3 PMID: 25216676
  44. Improved northern blot method for enhanced detection of small RNA.
    Nat Protoc. 2008;3(6):1077-84 PMID: 18536652
  45. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development.
    Genes Dev. 2004 May 15;18(10):1187-97 PMID: 15131082
  46. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends.
    Nat Biotechnol. 2008 Aug;26(8):941-6 PMID: 18542052
  47. Identification and functional characterization of tRNA-derived RNA fragments (tRFs) in respiratory syncytial virus infection.
    Mol Ther. 2013 Feb;21(2):368-79 PMID: 23183536
  48. Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae.
    Genetics. 2013 May;194(1):43-67 PMID: 23633143
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2017-05-19
Pages
5142-5152
Language
English
Region
England
NLM ID
0411011
PMCID
PMC5605234
Subset
IM
Grants
NIAID NIH HHS · R21 AI127582 · United States
NIGMS NIH HHS · T32 GM086252 · United States
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