Symptom Attenuation by a Normally Virulent Satellite RNA of Turnip Crinkle Virus Is Associated with the Coat Protein Open Reading Frame

Kong, Qingzhong; Oh, Jong-Won; Simon, Anne

doi:10.2307/3870024

Cited by 13 publications

(23 citation statements)

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“…Although the primary function of CP is structural, several studies have shown that it also has a vital role in virus-host interactions. This is supported from studies showing that certain TCV CP mutants cause altered symptom phenotypes (25) and that CP is responsible for modifying symptoms caused by satellite RNAs (31,32). In addition, it is well established that TCV CP is needed for systemic movement in most hosts, and cell-to-cell movement in Nicotiana benthamiana (20,34).…”

supporting

confidence: 51%

The Coat Protein of Turnip Crinkle Virus Suppresses Posttranscriptional Gene Silencing at an Early Initiation Step

Ren

Morris

2003

J Virol

284

269

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Posttranscriptional gene silencing (PTGS), or RNA silencing, is a sequence-specific RNA degradation process that targets foreign RNA, including viral and transposon RNA for destruction. Several RNA plant viruses have been shown to encode suppressors of PTGS in order to survive this host defense. We report here that the coat protein (CP) of Turnip crinkle virus (TCV) strongly suppresses PTGS. The Agrobacterium infiltration system was used to demonstrate that TCV CP suppressed the local PTGS as strongly as several previously reported virus-coded suppressors and that the action of TCV CP eliminated the small interfering RNAs associated with PTGS. We have also shown that the TCV CP must be present at the time of silencing initiation to be an effective suppressor. TCV CP was able to suppress PTGS induced by sense, antisense, and doublestranded RNAs, and it prevented systemic silencing. These data suggest that TCV CP functions to suppress RNA silencing at an early initiation step, likely by interfering the function of the Dicer-like RNase in plants.Posttranscriptional gene silencing (PTGS) is a sequencespecific RNA degradation process that leads to the elimination of the targeted RNA and loss of the function(s) encoded by the targeted RNA (1,6,62,69). This phenomenon was first observed and intensively studied in plant systems (see reference 64 for a review), where it has been associated with several processes, including cosuppression (44), repeat induced gene silencing (70), RNA-mediated resistance (35, 58), or homology-dependent gene silencing (43). Similar mechanisms were later discovered in other organisms, including quelling in filamentous fungus Neurospora crassa (9) and RNA interference (RNAi) in Caenorhabditis elegans (18) and Drosophila melanogaster (30). Recent research has revealed that all of these different phenomena have many common features and are now considered to be manifestations of an RNA-targeting pathway, whose natural functions include protecting hosts from invading viral RNAs and transposons (see references 45, 54, and 72 for reviews). RNA silencing has been proposed as a more general term to describe these related processes (1).Initiation and maintenance stages have been identified as distinct phases of the PTGS or RNA silencing process (10,50,65). In the initiation stage, the invading RNA triggers a pathway that results in its being degraded into a small RNA species of discrete size (21 to 25 nucleotides [nt]) called small interfering RNAs (siRNAs) that function as a guide for further degradation in the maintenance stage (22, 71). The most potent initiator of PTGS is thought to be double-stranded RNA (dsRNA) (8,18,30,68), although single-stranded RNA (ssRNA), both sense and antisense orientations, or even DNA trigger RNA silencing (15,65,66). ssRNA is most likely converted to a double-stranded form with the help of a host RNAdependent RNA polymerase (RdRP) in order to be effective (9,11,42,52,57). The dsRNA initiators are then degraded by an RNase III-like RNase (e.g., Dicer in Drosophila [3])...

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confidence: 51%

The Coat Protein of Turnip Crinkle Virus Suppresses Posttranscriptional Gene Silencing at an Early Initiation Step

Ren

Morris

2003

J Virol

284

269

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“…It was suggested that the highly structured nature of these subviral RNAs limited access by the RISC complex and this difference of accessibility accounted for preferential accumulation of the more highly structured smaller RNAs. In this context, the identification of suppressor activity associated with TCV CP provides a possible explanation for the observed role of the CP in modulating the effects of sat-RNA C on symptom development and satellite RNA accumulation [46].…”

Section: Some Common Features Of Virus-encoded Silencing Suppressorsmentioning

confidence: 99%

Suppressors of RNA silencing encoded by plant viruses and their role in viral infections

2005

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RNA silencing as a robust host defense mechanism against plant viruses is generally countered by virus-encoded silencing suppressors. This strategy is now increasingly recognized to be used by animal viruses as well. We present here an overview of the common features shared by some of the better studied plant viral silencing suppressors. We then briefly describe the characteristics of the few reported animal viral suppressors, notably their extraordinary ability of cross-kingdom suppression. We next discuss the basis for biased protection of viral RNA and subviral parasites by silencing suppressors, the link between movement and silencing suppression, the influence of temperature on the outcome of viral infection and the effect of viral silencing suppressors on the microRNA pathway.

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“…satC, by interfering with the replication of TCV in protoplasts (16) and accumulation in plants (20), was thought to fit that general description. However, the ability of satC to enhance the symptoms of TCV only in plants that display visible symptoms when infected with TCV alone suggested that the satRNA enhances the ability of the virus to colonize the plant and interact with cellular factors (20,54).…”

mentioning

confidence: 99%

Fitness of a Turnip Crinkle Virus Satellite RNA Correlates with a Sequence-Nonspecific Hairpin and Flanking Sequences That Enhance Replication and Repress the Accumulation of Virions

Sun

Simon

2003

J Virol

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Most plant viruses possess plus-sense single-stranded RNA genomes. Replication of these genomes is mediated by a replicase complex that in general comprises a virus-encoded RNA-dependent RNA polymerase (RdRp), other virally encoded proteins, and possibly host factors (17). The replicase must recognize its cognate RNA through direct or indirect interaction with specific cis-acting elements in the RNA template (4, 9), which for Brome mosaic virus are functional at various locations relative to the minus-strand initiation site (36). Replicases can accurately identify the correct start site for transcription of the genomic RNA, even when the site is artificially placed distal to the 3Ј end of the template (24,40,43). In addition, many viral RdRps synthesize 3Ј-coterminal subgenomic RNAs by using internal promoters located on minusstrand replication intermediates (18, 25, 48) that do not necessarily contain sequence or structural similarity to promoters that mediate full-length complementary-strand synthesis. Some plant viruses also provide the replication machinery for associated satellite RNAs (satRNAs), most of which share little sequence similarity with the viral genomic RNA (38). Thus, a single viral replicase must recognize a variety of seemingly different promoter elements.In addition to core promoter elements, many RNA virus genomes contain additional cis-acting elements that enhance but are not required for basal level transcription (29, 37). These RNA replication enhancers, which can be found in both plus and minus strands of viral RNAs, are located at variable positions in relation to the initiation site for RNA transcription and are thought to facilitate the recruitment of RdRp to the template (17). Replication enhancers have been characterized for a number of RNA viruses such as bacteriophage Q␤ (2), Alfalfa mosaic virus (46), Tomato bushy stunt virus (37), Brome mosaic virus (10,35,36), and Sindbis virus (11).Since most satRNAs associated with plant viruses are fewer than 500 bases in size and do not encode proteins, they are ideal templates for examining the structure and function of cis replication elements. The Turnip crinkle virus (TCV) (family Tombusviridae, genus Carmovirus) isolate TCV-M, a singlestranded RNA virus of 4,054 bases, was originally found to be associated with three related satRNAs, including satD (194 bases) and satC (356 bases) (1,22,39). satD appears to have originated from numerous short noncontiguous stretches of TCV genomic RNA sequence (5), while satC is a chimeric molecule containing nearly full-length satD at its 5Ј end and two discontinuous segments from TCV genomic RNA at its 3Ј end (Fig. 1A) (39). satC is also an unusually virulent satRNA, strongly intensifying the symptoms of TCV on hosts that display discernible symptoms when infected with TCV alone (20).Most satRNAs are considered to be parasitic agents, selfishly coopting the replication machinery of their helper virus without conferring any obvious advantage to the virus. satC, by interfering with the replication of ...

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Symptom Attenuation by a Normally Virulent Satellite RNA of Turnip Crinkle Virus Is Associated with the Coat Protein Open Reading Frame

Cited by 13 publications

References 0 publications

The Coat Protein of Turnip Crinkle Virus Suppresses Posttranscriptional Gene Silencing at an Early Initiation Step

The Coat Protein of Turnip Crinkle Virus Suppresses Posttranscriptional Gene Silencing at an Early Initiation Step

Suppressors of RNA silencing encoded by plant viruses and their role in viral infections

Fitness of a Turnip Crinkle Virus Satellite RNA Correlates with a Sequence-Nonspecific Hairpin and Flanking Sequences That Enhance Replication and Repress the Accumulation of Virions

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