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PMID: 30760640 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Control of Cognate Sense mRNA Translation by cis-Natural Antisense RNAs.

Plant physiology ·Vol. 180 ·No. 1 ·2019-00-00 ·Pages 305-322

Deforges J, Reis RS, Jacquet P, Sheppard S, Gadekar VP, Hart-Smith G, Tanzer A, Hofacker IL, Iseli C, Xenarios I, Poirier Y

Abstract

Cis-Natural Antisense Transcripts (cis-NATs), which overlap protein coding genes and are transcribed from the opposite DNA strand, constitute an important group of noncoding RNAs. Whereas several examples of cis-NATs regulating the expression of their cognate sense gene are known, most cis-NATs function by altering the steady-state level or structure of mRNA via changes in transcription, mRNA stability, or splicing, and very few cases involve the regulation of sense mRNA translation. This study was designed to systematically search for cis-NATs influencing cognate sense mRNA translation in Arabidopsis (Arabidopsis thaliana). Establishment of a pipeline relying on sequencing of total polyA+ and polysomal RNA from Arabidopsis grown under various conditions (i.e. nutrient deprivation and phytohormone treatments) allowed the identification of 14 cis-NATs whose expression correlated either positively or negatively with cognate sense mRNA translation. With use of a combination of cis-NAT stable over-expression in transgenic plants and transient expression in protoplasts, the impact of cis-NAT expression on mRNA translation was confirmed for 4 out of 5 tested cis-NAT:sense mRNA pairs. These results expand the number of cis-NATs known to regulate cognate sense mRNA translation and provide a foundation for future studies of their mode of action. Moreover, this study highlights the role of this class of noncoding RNAs in translation regulation.

MeSH Terms
Arabidopsis/genetics Arabidopsis Proteins/genetics DNA-Binding Proteins/genetics Gene Expression Regulation, Plant Plants, Genetically Modified Protein Biosynthesis RNA, Antisense/genetics RNA, Messenger/genetics RNA, Plant Reproducibility of Results Sequence Analysis, RNA Transcription Factors/genetics
Chemicals
Arabidopsis Proteins DNA-Binding Proteins RNA, Antisense RNA, Messenger RNA, Plant Transcription Factors WRKY45 protein, Arabidopsis
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Deforges Jules
Department of Plant Molecular Biology, University of Lausanne, Biophore Building, CH-1015 Lausanne, Switzerland.
Reis Rodrigo S ORCID
Department of Plant Molecular Biology, University of Lausanne, Biophore Building, CH-1015 Lausanne, Switzerland.
Jacquet Philippe
Department of Plant Molecular Biology, University of Lausanne, Biophore Building, CH-1015 Lausanne, Switzerland.
Sheppard Shaoline ORCID
Department of Plant Molecular Biology, University of Lausanne, Biophore Building, CH-1015 Lausanne, Switzerland.
Gadekar Veerendra P ORCID
Institute of Theoretical Chemistry, University of Vienna, Wahringer Str 17, A-1090 Vienna, Austria.
Hart-Smith Gene ORCID
School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney NSW 2052, Australia.
Tanzer Andrea ORCID
Institute of Theoretical Chemistry, University of Vienna, Wahringer Str 17, A-1090 Vienna, Austria.
Hofacker Ivo L ORCID
Institute of Theoretical Chemistry, University of Vienna, Wahringer Str 17, A-1090 Vienna, Austria.
Iseli Christian ORCID
Swiss Institute of Bioinformatics, CH-1015 Lausanne, Switzerland.
Xenarios Ioannis ORCID
Swiss Institute of Bioinformatics, CH-1015 Lausanne, Switzerland.
Poirier Yves ORCID
Department of Plant Molecular Biology, University of Lausanne, Biophore Building, CH-1015 Lausanne, Switzerland yves.poirier@unil.ch.
References (76)
76 references, click to expand
  1. New insights into nitric oxide signaling in plants.
    Annu Rev Plant Biol. 2008;59:21-39 PMID: 18031216
  2. Phylogeny-Based Systematization of Arabidopsis Proteins with Histone H1 Globular Domain.
    Plant Physiol. 2017 May;174(1):27-34 PMID: 28298478
  3. The H1 linker histones: multifunctional proteins beyond the nucleosomal core particle.
    EMBO Rep. 2015 Nov;16(11):1439-53 PMID: 26474902
  4. Assessment of selective mRNA translation in mammalian cells by polysome profiling.
    J Vis Exp. 2014 Oct 28;(92):e52295 PMID: 25407425
  5. The Arabidopsis information resource: Making and mining the "gold standard" annotated reference plant genome.
    Genesis. 2015 Aug;53(8):474-85 PMID: 26201819
  6. The functions and unique features of long intergenic non-coding RNA.
    Nat Rev Mol Cell Biol. 2018 Mar;19(3):143-157 PMID: 29138516
  7. A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness.
    Plant Cell. 2013 Oct;25(10):4166-82 PMID: 24096344
  8. Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20534-9 PMID: 19075248
  9. PLncDB: plant long non-coding RNA database.
    Bioinformatics. 2013 Apr 15;29(8):1068-71 PMID: 23476021
  10. HTSeq--a Python framework to work with high-throughput sequencing data.
    Bioinformatics. 2015 Jan 15;31(2):166-9 PMID: 25260700
  11. Conservation and functional element discovery in 20 angiosperm plant genomes.
    Mol Biol Evol. 2013 Jul;30(7):1729-44 PMID: 23640124
  12. Regulation of rice root development by a retrotransposon acting as a microRNA sponge.
    Elife. 2017 Aug 26;6: PMID: 28847366
  13. ELF18-INDUCED LONG-NONCODING RNA Associates with Mediator to Enhance Expression of Innate Immune Response Genes in Arabidopsis.
    Plant Cell. 2017 May;29(5):1024-1038 PMID: 28400491
  14. The long non-coding RNA GAS5 cooperates with the eukaryotic translation initiation factor 4E to regulate c-Myc translation.
    PLoS One. 2014 Sep 08;9(9):e107016 PMID: 25197831
  15. Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana.
    Genome Biol. 2005;6(4):R30 PMID: 15833117
  16. Mutually exclusive sense-antisense transcription at FLC facilitates environmentally induced gene repression.
    Nat Commun. 2016 Oct 07;7:13031 PMID: 27713408
  17. Regulation of transcription by long noncoding RNAs.
    Annu Rev Genet. 2014;48:433-55 PMID: 25251851
  18. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA.
    Science. 2011 Jan 7;331(6013):76-9 PMID: 21127216
  19. Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis.
    Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):E203-12 PMID: 24367078
  20. Long non-coding RNAs and their functions in plants.
    Curr Opin Plant Biol. 2015 Oct;27:207-16 PMID: 26342908
  21. Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis.
    Genes Dev. 2010 May 15;24(10):1010-21 PMID: 20478994
  22. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  23. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
    Nat Biotechnol. 2010 May;28(5):511-5 PMID: 20436464
  24. Long noncoding RNA modulates alternative splicing regulators in Arabidopsis.
    Dev Cell. 2014 Jul 28;30(2):166-76 PMID: 25073154
  25. Characterization of the RNA content of chromatin.
    Genome Res. 2010 Jul;20(7):899-907 PMID: 20404130
  26. Strigolactones are required for nitric oxide to induce root elongation in response to nitrogen and phosphate deficiencies in rice.
    Plant Cell Environ. 2016 Jul;39(7):1473-84 PMID: 27194103
  27. Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing.
    Science. 2010 Jan 1;327(5961):94-7 PMID: 19965720
  28. lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs.
    Nature. 2013 Aug 29;500(7464):598-602 PMID: 23945587
  29. Genome-wide view of natural antisense transcripts in Arabidopsis thaliana.
    DNA Res. 2015 Jun;22(3):233-43 PMID: 25922535
  30. The AS-RBM15 lncRNA enhances RBM15 protein translation during megakaryocyte differentiation.
    EMBO Rep. 2016 Jun;17(6):887-900 PMID: 27118388
  31. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
    Genome Biol. 2014;15(12):550 PMID: 25516281
  32. Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants.
    Plant Physiol. 2013 Apr;161(4):1875-84 PMID: 23429259
  33. Long noncoding RNA transcriptome of plants.
    Plant Biotechnol J. 2015 Apr;13(3):319-28 PMID: 25615265
  34. Landscape of transcription in human cells.
    Nature. 2012 Sep 6;489(7414):101-8 PMID: 22955620
  35. Regulatory roles of natural antisense transcripts.
    Nat Rev Mol Cell Biol. 2009 Sep;10(9):637-43 PMID: 19638999
  36. Systematic characterization of novel lncRNAs responding to phosphate starvation in Arabidopsis thaliana.
    BMC Genomics. 2016 Aug 18;17:655 PMID: 27538394
  37. Natural antisense transcripts.
    Hum Mol Genet. 2014 Sep 15;23(R1):R54-63 PMID: 24838284
  38. Extensive translation of small Open Reading Frames revealed by Poly-Ribo-Seq.
    Elife. 2014 Aug 21;3:e03528 PMID: 25144939
  39. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis.
    Nat Protoc. 2007;2(7):1565-72 PMID: 17585298
  40. Many lncRNAs, 5'UTRs, and pseudogenes are translated and some are likely to express functional proteins.
    Elife. 2015 Dec 19;4:e08890 PMID: 26687005
  41. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis.
    Nature. 2010 Apr 15;464(7291):1071-6 PMID: 20393566
  42. Target mimicry provides a new mechanism for regulation of microRNA activity.
    Nat Genet. 2007 Aug;39(8):1033-7 PMID: 17643101
  43. SINEs and LINEs: the art of biting the hand that feeds you.
    Curr Opin Cell Biol. 2002 Jun;14(3):343-50 PMID: 12067657
  44. FEELnc: a tool for long non-coding RNA annotation and its application to the dog transcriptome.
    Nucleic Acids Res. 2017 May 5;45(8):e57 PMID: 28053114
  45. Identification of antisense long noncoding RNAs that function as SINEUPs in human cells.
    Sci Rep. 2016 Sep 20;6:33605 PMID: 27646849
  46. COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction.
    Mol Plant. 2011 Jul;4(4):663-78 PMID: 21471330
  47. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat.
    Nature. 2012 Nov 15;491(7424):454-7 PMID: 23064229
  48. Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2008 Jun 24;105(25):8795-800 PMID: 18550839
  49. Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms.
    EMBO Rep. 2006 Dec;7(12):1216-22 PMID: 17139297
  50. Genome-wide assessment of differential translations with ribosome profiling data.
    Nat Commun. 2016 Apr 04;7:11194 PMID: 27041671
  51. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements.
    Nature. 2011 Feb 10;470(7333):284-8 PMID: 21307942
  52. Genome regulation by long noncoding RNAs.
    Annu Rev Biochem. 2012;81:145-66 PMID: 22663078
  53. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome.
    Plant J. 2017 Feb;89(4):789-804 PMID: 27862469
  54. A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana.
    Plant J. 2010 Feb 1;61(3):519-28 PMID: 19891705
  55. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes.
    Genes Dev. 2010 Oct 15;24(20):2264-9 PMID: 20952535
  56. Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis.
    Genome Res. 2014 Mar;24(3):444-53 PMID: 24402519
  57. Control of seed dormancy in Arabidopsis by a cis-acting noncoding antisense transcript.
    Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):E7846-E7855 PMID: 27856735
  58. Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation.
    Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):E10018-E10027 PMID: 29087317
  59. Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal.
    Dev Cell. 2013 Apr 15;25(1):69-80 PMID: 23541921
  60. The structure, organization and radiation of Sadhu non-long terminal repeat retroelements in Arabidopsis species.
    Mob DNA. 2010 Mar 01;1(1):10 PMID: 20226007
  61. Transcriptome analyses reveal SR45 to be a neutral splicing regulator and a suppressor of innate immunity in Arabidopsis thaliana.
    BMC Genomics. 2017 Oct 11;18(1):772 PMID: 29020934
  62. Super-resolution ribosome profiling reveals unannotated translation events in Arabidopsis.
    Proc Natl Acad Sci U S A. 2016 Nov 8;113(45):E7126-E7135 PMID: 27791167
  63. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor.
    Sci Signal. 2010 Feb 02;3(107):ra8 PMID: 20124551
  64. HISAT: a fast spliced aligner with low memory requirements.
    Nat Methods. 2015 Apr;12(4):357-60 PMID: 25751142
  65. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation.
    Mol Cell. 2010 Sep 24;39(6):925-38 PMID: 20797886
  66. PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element.
    Genes Dev. 2008 Aug 1;22(15):2085-92 PMID: 18676813
  67. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis.
    Proc Natl Acad Sci U S A. 2009 Nov 3;106(44):18843-8 PMID: 19843695
  68. Genome-wide identification and analysis of small RNAs originated from natural antisense transcripts in Oryza sativa.
    Genome Res. 2009 Jan;19(1):70-8 PMID: 18971307
  69. NERF encodes a RING E3 ligase important for drought resistance and enhances the expression of its antisense gene NFYA5 in Arabidopsis.
    Nucleic Acids Res. 2015 Jan;43(1):607-17 PMID: 25514924
  70. The Arabidopsis SWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility.
    Genome Biol. 2017 Jun 15;18(1):114 PMID: 28619072
  71. Evidence for natural antisense transcript-mediated inhibition of microRNA function.
    Genome Biol. 2010;11(5):R56 PMID: 20507594
  72. A transcription factor hierarchy defines an environmental stress response network.
    Science. 2016 Nov 4;354(6312): PMID: 27811239
  73. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus.
    Cell. 1992 Oct 30;71(3):515-26 PMID: 1423610
  74. Complementary Activities of TELOMERE REPEAT BINDING Proteins and Polycomb Group Complexes in Transcriptional Regulation of Target Genes.
    Plant Cell. 2016 Jan;28(1):87-101 PMID: 26721861
  75. Improved Quantitative Plant Proteomics via the Combination of Targeted and Untargeted Data Acquisition.
    Front Plant Sci. 2017 Sep 27;8:1669 PMID: 29021799
  76. LincRNA-p21 suppresses target mRNA translation.
    Mol Cell. 2012 Aug 24;47(4):648-55 PMID: 22841487
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2019-00-00
Epub
2019-00-13
Pages
305-322
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC6501089
Subset
IM
Analysis Services
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