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RNA Silencing in Aspergillus Nidulans Is Independent of RNA-Dependent RNA Polymerases

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RNA Silencing in Aspergillus Nidulans Is Independent of RNA-Dependent RNA Polymerases Copyright © 2005 by the Genetics Society of America DOI: 10.1534/genetics.104.035964 RNA Silencing in Aspergillus nidulans Is Independent of RNA-Dependent RNA Polymerases T. M. Hammond and N. P. Keller1 Department of Plant Pathology, University of Wisconsin, Madison, Wisconsin 53706 Manuscript received September 4, 2004 Accepted for publication November 5, 2004 ABSTRACT The versatility of RNA-dependent RNA polymerases (RDRPs) in eukaryotic gene silencing is perhaps best illustrated in the kingdom Fungi. Biochemical and genetic studies of Schizosaccharomyces pombe and Neurospora crassa show that these types of enzymes are involved in a number of fundamental gene-silencing processes, including heterochromatin regulation and RNA silencing in S. pombe and meiotic silencing and RNA silencing in N. crassa. Here we show that Aspergillus nidulans, another model fungus, does not require an RDRP for inverted repeat transgene (IRT)-induced RNA silencing. However, RDRP requirements may vary within the Aspergillus genus as genomic analysis indicates that A. nidulans, but not A. fumigatus or A. oryzae, has lost a QDE-1 ortholog, an RDRP associated with RNA silencing in N. crassa. We also provide evidence suggesting that 5Ј → 3Ј transitive RNA silencing is not a significant aspect of A. nidulans IRT- RNA silencing. These results indicate a lack of conserved kingdom-wide requirements for RDRPs in fungal RNA silencing. NA silencing refers to a group of very similar post- ases (RDRPs) are essential components of RNA silenc- R transcriptional gene-silencing mechanisms that ing (e.g., protists, nematodes; Smardon et al. 2000; Sijen have been discovered in a diverse range of eukaryotes et al. 2001; Martens et al. 2002; Simmer et al. 2002), (Pickford et al. 2002; Denli and Hannon 2003; Tang while in others RDRPs appear to be dispensable for this et al. 2003). The core processes of RNA silencing are process (e.g., flies, mammals; Schwarz et al. 2002; Stein highly conserved and involve double-stranded RNA et al. 2003). In plants and fungi, the roles of RDRPs in (dsRNA) processing by an RNAse III domain-containing RNA silencing are not as well defined. For example, the enzyme (Dicer) into 21- to 26-nt small interfering RNAs model plant A. thaliana encodes six putative RDRPs and (siRNAs; Bernstein et al. 2001), which are then incorpo- thus far only two have been partially investigated. Of rated into a ribonucleoprotein complex (RNA-induced these two RDRPs, SGS2/SDE1 is required for RNA si- silencing complex, RISC). RISC recognizes and de- lencing activated by sense transgenes (Beclin et al. grades target mRNAs by complementary base pairing 2002), but not for RNA silencing activated by inverted to the incorporated siRNA (Hammond et al. 2000; repeat transgenes (IRTs) or RNA viruses (Dalmay et al. Elbashir et al. 2001). An essential protein member of 2000; Beclin et al. 2002; Muangsan et al. 2004), and RISC is an argonaute family protein with a PAZ and AtRdRP1 is involved in viral defense (Yu et al. 2003; PIWI domain (PPD; Carmell et al. 2002). Examples Yang et al. 2004). include Rde-1 in Caenorhabditis elegans (Tabara et al. Studies of fungal RDRPs suggest that these enzymes 1999), dAgo2 in Drosophila melanogaster (Hammond et are involved in RNA silencing and a number of other al. 2001), Ago1 in Arabidopsis thaliana (Fagard et al. gene-silencing-related processes in fungi. For example, 2000), Ago1 in Schizosaccharomyces pombe (Volpe et al. the S. pombe RDRP, Rdp1, is required for RNA silencing 2002), and QDE-2 in Neurospora crassa (Catalanotto induced by IRTs (IRT-RNA silencing) and for RNAi- et al. 2002). Recent evidence suggests that the PAZ do- dependent heterochromatin formation at centromeric main of argonaute proteins facilitates transfer of siRNAs regions, mating-type loci, and euchromatic regions to the RISC complex (Lingel et al. 2003; Yan et al. 2003) (Volpe et al. 2002, 2003; Schramke and Allshire 2003; and that the PIWI domain contains the nuclease activity Jia et al. 2004; Verdel et al. 2004). While it is currently responsible for siRNA-guided mRNA cleavage (Song et unknown why the process of IRT-RNA silencing requires al. 2004). an RDRP in S. pombe, current models suggest that RNAi- In some organisms, RNA-dependent RNA polymer- dependent heterochromatin formation requires Rdp1 to create, directly or indirectly, small RNAs used to di- rect a complex of proteins, referred to as RNA-induced 1Corresponding author: Department of Plant Pathology, University of Wisconsin, 1630 Linden Dr., Madison, WI 53706. initiation of transcriptional gene silencing (RITS) pro- E-mail: [email protected] teins, to specific chromatin regions (Volpe et al. 2002, Genetics 169: 607–617 (February 2005) 608 T. M. Hammond and N. P. Keller 2003; Schramke and Allshire 2003; Verdel et al. upon IRT-RNA silencing while deletion of a putative 2004). PPD protein, named RsdA, disrupted this process. Possi- In the filamentous fungus N. crassa, there are two ble reasons to account for the apparent difference in a gene silencing processes that require two of three N. RDRP requirement for IRT-RNA silencing in S. pombe crassa RDRPs (Galagan et al. 2003). The first is N. crassa and A. nidulans are discussed. quelling, a type of RNA silencing that is thought to be related to high transgene number (Pickford et al. 2002; Forrest et al. 2004). This process requires the RDRP MATERIALS AND METHODS QDE-1 (Cogoni and Macino 1999a). In vitro studies of Strains, growth conditions, and transformation conditions: QDE-1 activity indicate that it produces both full-length All strains used in this study are listed in Table 1. A. nidulans complementary RNA (cRNA) and 9- to 21-nt cRNAs RJH0128 was transformed with aflR-specific IRTs and control along the length of single-stranded RNA templates transgenes using the method described by Yu and Adams (Makeyev and Bamford 2002), suggesting the possibil- (1999). Standard crossing techniques (Pontecorvo 1953) ity that QDE-1 creates dsRNA for processing by Dicer were then used to introduce different auxotrophic markers from A. nidulans RDIT1.1 into the aflR(IRT) and aflR single- or directly forms siRNAs for incorporation into RISC sense transgene (SST) transformants. Gene replacements during quelling (Makeyev and Bamford 2002). Such were confirmed by Southern blotting with probes specific for activities may be unnecessary when RNA silencing is the internal deleted region and at least one flanking region activated by IRTs, which may explain the recent finding of the deleted gene. A. nidulans RTMH13.C5 (for rsdA) and that QDE-1 is dispensable for IRT-RNA silencing (Cata- A. nidulans RTMH13.F5 (for rrpB and rrpC) were used as the hosts for gene replacements. A. nidulans cultures were grown lanotto et al. 2004). The second N. crassa gene-silenc- in 25 ml of appropriate supplemented liquid or solid minimal ing process requiring an RDRP is meiotic silencing by media or oatmeal agar as previously described (Butchko et unpaired DNA (MSUD; Shiu et al. 2001; Shiu and Met- al. 1999). All strains were cultured under dark, stationary Њ zenberg 2002). This process requires the RDRP SAD-1 conditions at 37 in standard Petri dishes. Liquid cultures were ϫ 6 ف (Shiu et al. 2001; Lee et al. 2003). A third N. crassa inoculated with 1 10 spores/ml and solid cultures were point inoculated with freshly harvested conidia. RDRP, RRP-3, has not yet been attributed with a func- Vector construction: Oligonucleotides used in vector con- tion. Phylogenetic analysis suggests RRP-3 is not part of struction are listed in Table 2. the quelling or MSUD pathways (Galagan et al. 2003; pTMH13.7 [also referred to as aflR(IRT1300)]: This transfor- bp-1300ف mation vector consists of an inverted repeat of two ف Borkovich et al. 2004) and biochemical studies suggests that it is not involved in DNA methylation or heterochro- aflR fragments (Figure 1) separated by an 280-bp spacer, driven by the A. nidulans gpdA promoter and terminated by matin formation (Freitag et al. 2004b). the A. nidulans trpC terminator (Punt et al. 1991). It also The zygomycete Mucor circinelloides may encode an contains a truncated A. nidulans trpC selectable marker for RDRP with an important role in transitive RNA silencing targeted integration of the IRT next to the A. nidulans trpC locus (Mullaney et al. 1985). Oligonucleotides aflh5-mod ف Nicolas et al. 2003). This process, more thoroughly) investigated in plants (Vaistij et al. 2002; Van Houdt and aflr3-BamHI were used to amplify an 1300-bp aflR frag- ment (5Ј HindIII-aflR), containing the full-length A. nidulans et al. 2003) and nematodes (Sijen et al. 2001), forms aflR coding sequence. This PCR product was cloned into the dsRNA/siRNAs from sequences upstream (3Ј → 5Ј) EcoRV site of pBluescript II SKϪ (pBS, Stratagene, La Jolla, and/or downstream (5Ј → 3Ј) of primary target se- CA) to create pTMH2.3. Oligonucleotides afln5-NcoI and aflr3-BamHI were then used to amplify a similar aflR fragment quences on targeted mRNA, leading to the creation of Ј Ј secondary siRNAs and the spreading of RNA silencing with a different restriction site in the 5 primer (5 NcoI-aflR). This PCR product was cloned into the SmaI site of pBS to create bp-1300ف Denli and Hannon 2003). In M. circinelloides these pTMH3.3. Using multiple cloning steps, these two) secondary siRNAs have been detected, but a specific aflR fragments were then placed in an inverted orientation bp spacer (gf1), creating plasmid-280ف RDRP has yet to be identified (Nicolas et al. 2003). on opposite sides of a Recently, a clear dissimilarity in fungal RDRP function pTMH8.7. The gf1 spacer was amplified from pPRgf-T4 (Zolo- became apparent when examination of a N.
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