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PMID: 16377568 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis.

Cell ·Vol. 123 ·No. 7 ·2005-12-29 ·Pages 1279-91

Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK

Abstract

In higher eukaryotes, miRNAs and siRNAs guide translational inhibition, mRNA cleavage, or chromatin regulation. We found that the antisense overlapping gene pair of Delta(1)-pyrroline-5-carboxylate dehydrogenase (P5CDH), a stress-related gene, and SRO5, a gene of unknown function, generates two types of siRNAs. When both transcripts are present, a 24-nt siRNA is formed by a biogenesis pathway dependent on DCL2, RDR6, SGS3, and NRPD1A. Initial cleavage of the P5CDH transcript guided by the 24-nt siRNA establishes a phase for the subsequent generation of 21-nt siRNAs by DCL1 and further cleavage of P5CDH transcripts. The expression of SRO5 is induced by salt, and this induction is required to initiate siRNA formation. Our data suggest that the P5CDH and SRO5 proteins are also functionally related, and that the P5CDH-SRO5 gene pair defines a mode of siRNA function and biogenesis that may be applied to other natural cis-antisense gene pairs in eukaryotic genomes.

MeSH Terms
1-Pyrroline-5-Carboxylate Dehydrogenase/genetics,metabolism Arabidopsis/drug effects,genetics,physiology Arabidopsis Proteins/genetics,metabolism Base Sequence Down-Regulation/drug effects,physiology Models, Biological Molecular Sequence Data Mutation Proline/metabolism RNA, Antisense/genetics RNA, Small Interfering/biosynthesis,physiology Salts/metabolism,pharmacology Up-Regulation/drug effects,physiology
Chemicals
Arabidopsis Proteins RNA, Antisense RNA, Small Interfering Salts Proline 1-Pyrroline-5-Carboxylate Dehydrogenase ALDH12A1 protein, Arabidopsis
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Borsani Omar
Institute for Integrative Genome Biology and Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA.
Zhu Jianhua
Verslues Paul E
Sunkar Ramanjulu
Zhu Jian-Kang
References (50)
50 references, click to expand
  1. MicroRNA pathways in flies and worms: growth, death, fat, stress, and timing.
    Cell. 2003 Jun 13;113(6):673-6 PMID: 12809598
  2. Role of microRNAs in plant and animal development.
    Science. 2003 Jul 18;301(5631):336-8 PMID: 12869753
  3. The small RNA profile during Drosophila melanogaster development.
    Dev Cell. 2003 Aug;5(2):337-50 PMID: 12919683
  4. Control of leaf morphogenesis by microRNAs.
    Nature. 2003 Sep 18;425(6955):257-63 PMID: 12931144
  5. Asymmetry in the assembly of the RNAi enzyme complex.
    Cell. 2003 Oct 17;115(2):199-208 PMID: 14567917
  6. Functional siRNAs and miRNAs exhibit strand bias.
    Cell. 2003 Oct 17;115(2):209-16 PMID: 14567918
  7. Empirical analysis of transcriptional activity in the Arabidopsis genome.
    Science. 2003 Oct 31;302(5646):842-6 PMID: 14593172
  8. MicroRNAs: genomics, biogenesis, mechanism, and function.
    Cell. 2004 Jan 23;116(2):281-97 PMID: 14744438
  9. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation.
    Proc Natl Acad Sci U S A. 2004 Jan 27;101(4):1093-8 PMID: 14722360
  10. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing.
    Curr Biol. 2004 Feb 17;14(4):346-51 PMID: 14972688
  11. Genetic and functional diversification of small RNA pathways in plants.
    PLoS Biol. 2004 May;2(5):E104 PMID: 15024409
  12. Hydrogen peroxide mediates plant root cell response to nutrient deprivation.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8827-32 PMID: 15173595
  13. MicroRNAs in plants.
    Genes Dev. 2002 Jul 1;16(13):1616-26 PMID: 12101121
  14. A plant gene up-regulated at rust infection sites.
    Plant Physiol. 2002 May;129(1):169-80 PMID: 12011348
  15. A biochemical framework for RNA silencing in plants.
    Genes Dev. 2003 Jan 1;17(1):49-63 PMID: 12514099
  16. DICER-LIKE1: blind men and elephants in Arabidopsis development.
    Trends Plant Sci. 2002 Nov;7(11):487-91 PMID: 12417148
  17. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA.
    Science. 2002 Sep 20;297(5589):2053-6 PMID: 12242443
  18. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi.
    Science. 2002 Sep 13;297(5588):1833-7 PMID: 12193640
  19. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana.
    Curr Biol. 2002 Sep 3;12(17):1484-95 PMID: 12225663
  20. Salt and drought stress signal transduction in plants.
    Annu Rev Plant Biol. 2002;53:247-73 PMID: 12221975
  21. Two classes of short interfering RNA in RNA silencing.
    EMBO J. 2002 Sep 2;21(17):4671-9 PMID: 12198169
  22. RNA interference.
    Nature. 2002 Jul 11;418(6894):244-51 PMID: 12110901
  23. A nuclear gene encoding mitochondrial Delta-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity.
    Plant J. 2001 Aug;27(4):345-56 PMID: 11532180
  24. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs.
    Curr Biol. 2005 Aug 23;15(16):1494-500 PMID: 16040244
  25. Natural antisense transcripts with coding capacity in Arabidopsis may have a regulatory role that is not linked to double-stranded RNA degradation.
    Genome Biol. 2005;6(6):R51 PMID: 15960803
  26. microRNA-directed phasing during trans-acting siRNA biogenesis in plants.
    Cell. 2005 Apr 22;121(2):207-21 PMID: 15851028
  27. DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis.
    Curr Biol. 2000 Dec 14-28;10(24):1591-4 PMID: 11137011
  28. Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application.
    Plant Physiol. 2000 Jun;123(2):779-89 PMID: 10859207
  29. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance.
    Cell. 2000 May 26;101(5):533-42 PMID: 10850495
  30. Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays.
    Nat Biotechnol. 2000 Jun;18(6):630-4 PMID: 10835600
  31. A species of small antisense RNA in posttranscriptional gene silencing in plants.
    Science. 1999 Oct 29;286(5441):950-2 PMID: 10542148
  32. RNA silencing genes control de novo DNA methylation.
    Science. 2004 Feb 27;303(5662):1336 PMID: 14988555
  33. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis.
    Genes Dev. 2005 Sep 15;19(18):2164-75 PMID: 16131612
  34. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12984-9 PMID: 16129836
  35. Elucidation of the small RNA component of the transcriptome.
    Science. 2005 Sep 2;309(5740):1567-9 PMID: 16141074
  36. MicroRNAs: small RNAs with a big role in gene regulation.
    Nat Rev Genet. 2004 Jul;5(7):522-31 PMID: 15211354
  37. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses.
    Plant Cell. 2004 Jul;16(7):1925-37 PMID: 15208394
  38. Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats.
    Curr Biol. 2004 Jul 13;14(13):1214-20 PMID: 15242620
  39. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2001-19 PMID: 15258262
  40. Role of the yeast acetyltransferase Mpr1 in oxidative stress: regulation of oxygen reactive species caused by a toxic proline catabolism intermediate.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12616-21 PMID: 15308773
  41. Mechanisms of gene silencing by double-stranded RNA.
    Nature. 2004 Sep 16;431(7006):343-9 PMID: 15372041
  42. RNA silencing in plants.
    Nature. 2004 Sep 16;431(7006):356-63 PMID: 15372043
  43. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis.
    Genes Dev. 2004 Oct 1;18(19):2368-79 PMID: 15466488
  44. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs.
    Mol Cell. 2004 Oct 8;16(1):69-79 PMID: 15469823
  45. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana.
    Nat Genet. 2004 Dec;36(12):1282-90 PMID: 15565108
  46. The role of [Delta]1-pyrroline-5-carboxylate dehydrogenase in proline degradation.
    Plant Cell. 2004 Dec;16(12):3413-25 PMID: 15548746
  47. Global identification of human transcribed sequences with genome tiling arrays.
    Science. 2004 Dec 24;306(5705):2242-6 PMID: 15539566
  48. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation.
    Cell. 2005 Mar 11;120(5):613-22 PMID: 15766525
  49. RNA polymerase IV directs silencing of endogenous DNA.
    Science. 2005 Apr 1;308(5718):118-20 PMID: 15692015
  50. Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana.
    Genome Biol. 2005;6(4):R30 PMID: 15833117
Article Info
Journal
Cell
Abbr.
Cell
ISSN
0092-8674
Published
2005-12-29
Pages
1279-91
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3137516
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059138 · United States
NIGMS NIH HHS · R01 GM059138-11 · United States
NIGMS NIH HHS · R01GM0707501 · United States
NIGMS NIH HHS · R01GM59138 · United States
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