Home LiteratureArticle Details
PMID: 18003861 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A novel class of bacteria-induced small RNAs in Arabidopsis.

Genes & development ·Vol. 21 ·No. 23 ·2007-12-01 ·Pages 3123-34

Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H

Abstract

Small RNAs, including microRNAs (miRNAs) and small interfering RNAs (siRNAs), are essential regulatory molecules of many cellular processes. Arabidopsis has at least three classes of endogenous siRNAs--chromatin-associated siRNAs, trans-acting siRNAs (tasiRNAs), and natural antisense transcript (NAT)-associated siRNAs (nat-siRNAs)--all 20-25 nucleotides (nt) in length. Here, we identified a novel class of small RNAs, long siRNAs (lsiRNAs), which are 30-40 nt and share many common features with known siRNAs. The lsiRNAs identified so far are induced by pathogen infection or under specific growth conditions. One of the lsiRNAs, AtlsiRNA-1, is generated from SRRLK/AtRAP NAT pair and specifically induced by the bacterium Pseudomonas syringae carrying effector avrRpt2. Recently, 25- to 31-nt PIWI-interacting RNAs (piRNAs) and repeat-associated siRNAs (rasiRNAs) were identified in animal germline cells. In contrast to the biogenesis of piRNAs/rasiRNAs, which is dicer independent and requires PIWI subfamily proteins, generation of AtlsiRNA-1 requires DCL1, DCL4, and the ARGONAUTE subfamily protein AGO7. It also depends on HYL1, HEN1, HST1, RDR6, and Pol IV. Induction of AtlsiRNA-1 silences AtRAP, which encodes a RAP-domain protein involved in disease resistance. Our further analysis implies that AtlsiRNA-1 may destabilize target mRNA through decapping and XRN4-mediated 5'-to-3' degradation.

MeSH Terms
Animals Arabidopsis/genetics,metabolism,microbiology Arabidopsis Proteins/genetics Gene Expression Regulation, Plant Genes, Plant MicroRNAs/biosynthesis,classification,genetics Plant Diseases/genetics,microbiology Pseudomonas syringae/genetics,pathogenicity RNA Stability RNA, Small Interfering/biosynthesis,classification,genetics
Chemicals
Arabidopsis Proteins MicroRNAs RNA, Small Interfering
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Katiyar-Agarwal Surekha
Department of Plant Pathology and Microbiology, Center for Plant Cell Biology and Institute for Integrative Genome Biology, University of California at Riverside, Riverside, California 92521, USA.
Gao Shang
Vivian-Smith Adam
Jin Hailing
References (61)
61 references, click to expand
  1. Small RNA-mediated chromatin silencing directed to the 3' region of the Arabidopsis gene encoding the developmental regulator, FLC.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3633-8 PMID: 17360694
  2. Elucidation of the small RNA component of the transcriptome.
    Science. 2005 Sep 2;309(5740):1567-9 PMID: 16141074
  3. Methylation as a crucial step in plant microRNA biogenesis.
    Science. 2005 Feb 11;307(5711):932-5 PMID: 15705854
  4. Components of the Arabidopsis mRNA decapping complex are required for early seedling development.
    Plant Cell. 2007 May;19(5):1549-64 PMID: 17513503
  5. Role of RNA polymerase IV in plant small RNA metabolism.
    Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4536-41 PMID: 17360559
  6. Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development.
    Plant Cell. 2006 Dec;18(12):3386-98 PMID: 17158604
  7. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome.
    Genes Dev. 2006 Aug 15;20(16):2214-22 PMID: 16882972
  8. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline.
    Curr Biol. 2001 Jul 10;11(13):1017-27 PMID: 11470406
  9. The developmental timing regulator AIN-1 interacts with miRISCs and may target the argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans.
    Mol Cell. 2005 Aug 19;19(4):437-47 PMID: 16109369
  10. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs.
    Science. 2006 Apr 7;312(5770):75-9 PMID: 16484454
  11. A germline-specific class of small RNAs binds mammalian Piwi proteins.
    Nature. 2006 Jul 13;442(7099):199-202 PMID: 16751776
  12. A pathogen-inducible endogenous siRNA in plant immunity.
    Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):18002-7 PMID: 17071740
  13. Arabidopsis endogenous small RNAs: highways and byways.
    Trends Plant Sci. 2006 Sep;11(9):460-8 PMID: 16893673
  14. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis.
    Curr Biol. 2006 May 9;16(9):939-44 PMID: 16682356
  15. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes.
    PLoS One. 2007 Feb 14;2(2):e219 PMID: 17299599
  16. AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets.
    Mol Cell. 2004 Jul 23;15(2):173-83 PMID: 15260969
  17. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis.
    Cell. 2005 Dec 29;123(7):1279-91 PMID: 16377568
  18. Discovery of pathogen-regulated small RNAs in plants.
    Methods Enzymol. 2007;427:215-27 PMID: 17720487
  19. Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana.
    Genome Biol. 2005;6(4):R30 PMID: 15833117
  20. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies.
    Nat Cell Biol. 2005 Jul;7(7):719-23 PMID: 15937477
  21. RNA silencing in plants.
    Nature. 2004 Sep 16;431(7006):356-63 PMID: 15372043
  22. ASRP: the Arabidopsis Small RNA Project Database.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D637-40 PMID: 15608278
  23. Maintenance of genomic methylation requires a SWI2/SNF2-like protein.
    Nat Genet. 1999 May;22(1):94-7 PMID: 10319870
  24. AtPARN is an essential poly(A) ribonuclease in Arabidopsis.
    Gene. 2004 Mar 17;328:95-102 PMID: 15019988
  25. DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7.
    Curr Biol. 2006 May 9;16(9):927-32 PMID: 16682354
  26. A novel class of small RNAs bind to MILI protein in mouse testes.
    Nature. 2006 Jul 13;442(7099):203-7 PMID: 16751777
  27. A novel class of small RNAs in mouse spermatogenic cells.
    Genes Dev. 2006 Jul 1;20(13):1709-14 PMID: 16766680
  28. The small RNA profile during Drosophila melanogaster development.
    Dev Cell. 2003 Aug;5(2):337-50 PMID: 12919683
  29. A link between mRNA turnover and RNA interference in Arabidopsis.
    Science. 2004 Nov 5;306(5698):1046-8 PMID: 15528448
  30. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis.
    Plant Cell. 2004 Aug;16(8):2001-19 PMID: 15258262
  31. Characterization of the piRNA complex from rat testes.
    Science. 2006 Jul 21;313(5785):363-7 PMID: 16778019
  32. Genome-wide profiling and analysis of Arabidopsis siRNAs.
    PLoS Biol. 2007 Mar;5(3):e57 PMID: 17298187
  33. Conjugation-specific small RNAs in Tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement.
    Genes Dev. 2004 Sep 1;18(17):2068-73 PMID: 15314029
  34. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila.
    Cell. 2007 Mar 23;128(6):1089-103 PMID: 17346786
  35. Control of translation and mRNA degradation by miRNAs and siRNAs.
    Genes Dev. 2006 Mar 1;20(5):515-24 PMID: 16510870
  36. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway.
    Curr Biol. 2006 May 9;16(9):933-8 PMID: 16682355
  37. Gateway-compatible vectors for plant functional genomics and proteomics.
    Plant J. 2006 Feb;45(4):616-29 PMID: 16441352
  38. Two classes of endogenous small RNAs in Tetrahymena thermophila.
    Genes Dev. 2006 Jan 1;20(1):28-33 PMID: 16357212
  39. Ribo-gnome: the big world of small RNAs.
    Science. 2005 Sep 2;309(5740):1519-24 PMID: 16141061
  40. Genome sequencing in microfabricated high-density picolitre reactors.
    Nature. 2005 Sep 15;437(7057):376-80 PMID: 16056220
  41. A distinct small RNA pathway silences selfish genetic elements in the germline.
    Science. 2006 Jul 21;313(5785):320-4 PMID: 16809489
  42. Distinct expression patterns of natural antisense transcripts in Arabidopsis.
    Plant Physiol. 2007 Jul;144(3):1247-55 PMID: 17496106
  43. Host-microbe interactions: shaping the evolution of the plant immune response.
    Cell. 2006 Feb 24;124(4):803-14 PMID: 16497589
  44. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish.
    Cell. 2007 Apr 6;129(1):69-82 PMID: 17418787
  45. Nomenclature and functions of RNA-directed RNA polymerases.
    Trends Plant Sci. 2006 Mar;11(3):142-51 PMID: 16473542
  46. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila.
    Science. 2007 Mar 16;315(5818):1587-90 PMID: 17322028
  47. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes.
    Genes Dev. 2006 Jul 15;20(14):1885-98 PMID: 16815998
  48. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana.
    Genes Dev. 2006 Dec 15;20(24):3407-25 PMID: 17182867
  49. Endogenous and silencing-associated small RNAs in plants.
    Plant Cell. 2002 Jul;14(7):1605-19 PMID: 12119378
  50. The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated.
    Nat Struct Mol Biol. 2007 Apr;14(4):349-50 PMID: 17384646
  51. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies.
    Nat Cell Biol. 2005 Jun;7(6):633-6 PMID: 15908945
  52. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena.
    Cell. 2002 Sep 20;110(6):689-99 PMID: 12297043
  53. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  54. MicroRNAs direct rapid deadenylation of mRNA.
    Proc Natl Acad Sci U S A. 2006 Mar 14;103(11):4034-9 PMID: 16495412
  55. SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis.
    EMBO J. 2001 Apr 17;20(8):2069-78 PMID: 11296239
  56. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center.
    Cell. 2006 Jul 14;126(1):79-92 PMID: 16839878
  57. A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase.
    Genes Dev. 2005 Jan 1;19(1):77-89 PMID: 15598983
  58. Mouse Piwi-interacting RNAs are 2'-O-methylated at their 3' termini.
    Nat Struct Mol Biol. 2007 Apr;14(4):347-8 PMID: 17384647
  59. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling.
    Science. 2006 Apr 21;312(5772):436-9 PMID: 16627744
  60. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana.
    Cell. 2006 Jul 14;126(1):93-106 PMID: 16839879
  61. zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline.
    Dev Cell. 2007 Jun;12(6):851-62 PMID: 17543859
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
DOI
10.1101/gad.1595107
Published
2007-12-01
Epub
2007-00-14
Pages
3123-34
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC2081978
Subset
IM
External Links
PubMed source DOI: 10.1101/gad.1595107 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2