Abstract
RNA interference pathways use small RNAs to mediate gene silencing in eukaryotes. In addition to small interfering RNAs (siRNAs) and microRNAs, several types of endogenously produced small RNAs have important roles in gene regulation, germ cell maintenance and transposon silencing. The production of some of these RNAs requires the synthesis of aberrant RNAs (aRNAs) or pre-siRNAs, which are specifically recognized by RNA-dependent RNA polymerases to make double-stranded RNA. The mechanism for aRNA synthesis and recognition is largely unknown. Here we show that DNA damage induces the expression of the Argonaute protein QDE-2 and a new class of small RNAs in the filamentous fungus Neurospora crassa. This class of small RNAs, known as qiRNAs because of their interaction with QDE-2, are about 20-21 nucleotides long (several nucleotides shorter than Neurospora siRNAs), with a strong preference for uridine at the 5' end, and originate mostly from the ribosomal DNA locus. The production of qiRNAs requires the RNA-dependent RNA polymerase QDE-1, the Werner and Bloom RecQ DNA helicase homologue QDE-3 and dicers. qiRNA biogenesis also requires DNA-damage-induced aRNAs as precursors, a process that is dependent on both QDE-1 and QDE-3. Notably, our results suggest that QDE-1 is the DNA-dependent RNA polymerase that produces aRNAs. Furthermore, the Neurospora RNA interference mutants show increased sensitivity to DNA damage, suggesting a role for qiRNAs in the DNA-damage response by inhibiting protein translation.
MeSH Terms
DNA Damage/genetics
DNA Helicases/genetics,metabolism
DNA, Ribosomal/genetics
DNA, Single-Stranded
Fungal Proteins/biosynthesis,genetics,metabolism
Gene Expression Regulation, Fungal
Molecular Sequence Data
Neurospora crassa/enzymology,genetics
Protein Biosynthesis
RNA, Fungal/biosynthesis,genetics,metabolism
RNA, Small Interfering/biosynthesis,genetics,metabolism
RNA-Dependent RNA Polymerase/genetics,metabolism
Templates, Genetic
Chemicals
DNA, Ribosomal
DNA, Single-Stranded
Fungal Proteins
QDE-2 protein, Neurospora crassa
RNA, Fungal
RNA, Small Interfering
QDE1 protein, Neurospora crassa
RNA-Dependent RNA Polymerase
DNA Helicases
QDE-3 protein, Neurospora crassa
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Lee Heng-Chi
Department of Physiology, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, Texas 75390, USA.
Chang Shwu-Shin
Choudhary Swati
Aalto Antti P
Maiti Mekhala
Bamford Dennis H
Liu Yi
References (31)
31 references, click to expand
-
A double-stranded-RNA response program important for RNA interference efficiency.
Mol Cell Biol. 2007 Jun;27(11):3995-4005
PMID: 17371837
-
Involvement of small RNAs and role of the qde genes in the gene silencing pathway in Neurospora.
Genes Dev. 2002 Apr 1;16(7):790-5
PMID: 11937487
-
RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing.
Genes Dev. 2005 Oct 1;19(19):2301-6
PMID: 16204182
-
Cellular RNA-dependent RNA polymerase involved in posttranscriptional gene silencing has two distinct activity modes.
Mol Cell. 2002 Dec;10(6):1417-27
PMID: 12504016
-
H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability.
Nat Cell Biol. 2007 Jan;9(1):25-35
PMID: 17159999
-
QIP, a putative exonuclease, interacts with the Neurospora Argonaute protein and facilitates conversion of duplex siRNA into single strands.
Genes Dev. 2007 Mar 1;21(5):590-600
PMID: 17311884
-
RNA interference.
Nature. 2002 Jul 11;418(6894):244-51
PMID: 12110901
-
The RNA-dependent RNA polymerase essential for post-transcriptional gene silencing in Neurospora crassa interacts with replication protein A.
Nucleic Acids Res. 2008 Feb;36(2):532-8
PMID: 18048414
-
RNA polymerase IV directs silencing of endogenous DNA.
Science. 2005 Apr 1;308(5718):118-20
PMID: 15692015
-
piRNAs in the germ line.
Science. 2007 Apr 20;316(5823):397
PMID: 17446387
-
Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints.
Annu Rev Biochem. 2004;73:39-85
PMID: 15189136
-
Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation.
Cell. 2005 Mar 11;120(5):613-22
PMID: 15766525
-
Superoxide dismutase (sod-1) null mutants of Neurospora crassa: oxidative stress sensitivity, spontaneous mutation rate and response to mutagens.
Genetics. 1994 Jul;137(3):723-30
PMID: 8088518
-
Perspective: machines for RNAi.
Genes Dev. 2005 Mar 1;19(5):517-29
PMID: 15741316
-
Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase.
Nature. 1999 May 13;399(6732):166-9
PMID: 10335848
-
Deoxyribonucleoside triphosphate pools in Neurospora crassa: effects of histidine and hydroxyurea.
Mutat Res. 1988 Jul-Aug;200(1-2):45-53
PMID: 2969078
-
Small silencing RNAs: an expanding universe.
Nat Rev Genet. 2009 Feb;10(2):94-108
PMID: 19148191
-
Characterization of the piRNA complex from rat testes.
Science. 2006 Jul 21;313(5785):363-7
PMID: 16778019
-
RNA polymerase II is required for RNAi-dependent heterochromatin assembly.
Science. 2005 Jul 15;309(5733):467-9
PMID: 15947136
-
The structure of an RNAi polymerase links RNA silencing and transcription.
PLoS Biol. 2006 Dec;4(12):e434
PMID: 17147473
-
An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans.
Science. 2001 Oct 26;294(5543):858-62
PMID: 11679671
-
Relationship of histidine sensitivity to DNA damage and stress induced responses in mutagen sensitive mutants of Neurospora crassa.
Curr Genet. 1988 May;13(5):391-9
PMID: 2969780
-
Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase.
Science. 1999 Dec 17;286(5448):2342-4
PMID: 10600745
-
Characterization of the short RNAs bound by the P19 suppressor of RNA silencing in mouse embryonic stem cells.
RNA. 2006 Dec;12(12):2092-102
PMID: 17135486
-
Homology effects in Neurospora crassa.
FEMS Microbiol Lett. 2006 Jan;254(2):182-9
PMID: 16445744
-
Gene silencing in worms and fungi.
Nature. 2000 Mar 16;404(6775):245
PMID: 10749199
-
Biochemical activities of Arabidopsis RNA-dependent RNA polymerase 6.
J Biol Chem. 2008 Feb 8;283(6):3059-3066
PMID: 18063577
-
The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center.
Cell. 2006 Jul 14;126(1):79-92
PMID: 16839878
-
Replicase activity of purified recombinant protein P2 of double-stranded RNA bacteriophage phi6.
EMBO J. 2000 Jan 4;19(1):124-33
PMID: 10619851
-
Transcription and RNAi in heterochromatic gene silencing.
Nat Struct Mol Biol. 2007 Nov;14(11):1041-8
PMID: 17984966
-
Redundancy of the two dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa.
Mol Cell Biol. 2004 Mar;24(6):2536-45
PMID: 14993290