Host-specific encapsidation of a defective RNA 3 of Cucumber mosaic virus

Kaplan, Igor B.; Lee, Kian-Chung; Canto, Tomás; Wong, Sek‐Man; Palukaitis, Peter

doi:10.1099/vir.0.80345-0

Cited by 11 publications

(9 citation statements)

References 26 publications

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“…It was shown previously that DI RNA was encapsidated (16); however, it may be that the DI particles (or DI RNA) are unable to bind to the necessary virus or host factors required for long-distance movement (11,13). Similar observations were also reported in other studies involving CMV and different hosts as CMV D RNA accumulated in upper leaves of Nicotiana species but did not move systemically in muskmelon, tomato, or zucchini squash (7,8). Therefore, it is also possible that the capacity of DI RNA to move efficiently is host dependent, and the mechanism of inhibition of DI long-distance movement remains to be studied.…”

Section: Discussionsupporting

confidence: 76%

“…Although the DI RNA could represent up to 60% of virusspecific RNA in the infected plants, as in case of tombusviruses, the percentage of encapsidated DI RNAs could be as low as 3 to 4%, and most DI RNAs are not transmitted by vectors (1,2,6). Moreover, while most DI RNAs can efficiently accumulate in inoculated tissue, they do not always move systemically, as exempli-fied by cucumber mosaic virus (CMV) D RNA, which moves long distances in tobacco species but not in tomato, zucchini squash, or muskmelon (1,7,8).…”

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confidence: 99%

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Deciphering the Mechanism of Defective Interfering RNA (DI RNA) Biogenesis Reveals That a Viral Protein and the DI RNA Act Antagonistically in Virus Infection

Lukhovitskaya

Thaduri

Garushyants

et al. 2013

J Virol

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Virus accumulation was reduced when the 8K ORF was disrupted but D RNA was produced. Conversely, the virus accumulated at higher titers when the 8K ORF was intact and D RNA production was blocked. These data demonstrate that the D RNA interferes with virus infection and therefore should be referred to as a defective interfering RNA (DI RNA). The 8K protein was shown to be a weak silencing suppressor. This study provides an example of the interplay between a pathogen and its molecular parasite where virus accumulation was differentially regulated by the 8K protein and DI RNA, indicating that they play antagonistic roles and suggesting a mechanism by which the virus can attenuate replication, decreasing viral load and thereby enhancing its efficiency as a parasite.T he small genome size of RNA viruses means that most viral proteins are multifunctional and that viruses adopt several different strategies for gene expression including overlapping open reading frames (ORFs). In the course of infection many RNA viruses produce defective RNAs (D RNAs), which are deleted versions of the viral genome (see references 1 and 2 for a review). Because they lack essential genetic information, in plants D RNAs are totally dependent on the infectious helper virus for replication, encapsidation, and cell-to-cell and long-distance movement. Interference occurs when D RNA reduces symptom production by the parent virus or/and reduces multiplication of the helper virus; hence, the term defective interfering RNA (DI RNA) is used.Production of D RNA molecules during replication cycles seems to be a common occurrence in many viruses. D and DI RNAs of plant viruses, including DNA and negative-and positivestranded RNA viruses, have been described and characterized previously (1, 2). In some instances, for example, the criniviruses, DI RNAs consist of a mosaic of the multipartite parental viral genome (3). Multiple-deletion DI RNAs are typical for several members of genus Tombusvirus, and these DI RNAs have been extensively studied (4, 5). On the other hand, single-deletion D and DI RNAs have been reported in Potexvirus and Tobravirus genera as well as in several soilborne viruses of the genera Furo-, and Benyvirus (1).Although the DI RNA could represent up to 60% of virusspecific RNA in the infected plants, as in case of tombusviruses, the percentage of encapsidated DI RNAs could be as low as 3 to 4%, and most DI RNAs are not transmitted by vectors (1, 2, 6). Moreover, while most DI RNAs can efficiently accumulate in inoculated tissue, they do not always move systemically, as exemplified by cucumber mosaic virus (CMV) D RNA, which moves long distances in tobacco species but not in tomato, zucchini squash, or muskmelon (1,7,8).Three major mechanisms of interference by DI RNAs have been recognized (reviewed in references 2 and 5). These mechanisms are the following: (i) competition for viral and host resources, which impairs virus replication and attenuates the symptoms; (ii) DI RNA-triggered gene-silencing response; (iii) modulation of the...

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Section: Discussionsupporting

confidence: 76%

mentioning

confidence: 99%

Deciphering the Mechanism of Defective Interfering RNA (DI RNA) Biogenesis Reveals That a Viral Protein and the DI RNA Act Antagonistically in Virus Infection

Lukhovitskaya

Thaduri

Garushyants

et al. 2013

J Virol

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“…Replicase errors and RNA recombination are also responsible for the formation of defective RNAs, the deleted forms of viral RNAs that contain portions of the parental virus genome (21). For instance, the ability of defective RNA to replicate and to interfere with genomic BMV RNA replication has been demonstrated for barley (21,22) and for zucchini (52) protoplasts.…”

Section: Genetic Recombination Of Bromoviridaementioning

confidence: 99%

Insights into the Single-Cell Reproduction Cycle of Members of the Family Bromoviridae : Lessons from the Use of Protoplast Systems

Sztuba-Solińska

Bujarski

2008

J Virol

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2The development of single-cell protoplast systems is certainly one of the milestones in the history of plant virology, allowing for the analysis of viral molecular processes at the cellular level. The use of plant cell-based systems in the study of the Bromoviridae family of multipartite single-stranded plant RNA viruses facilitated the discovery and dissection of viral processes engaged in the single-cell reproduction cycle: replication, transcription, protein synthesis, movement, virion assembly, and RNA recombination. This review summarizes the application of protoplast systems to the analysis of consecutive steps of the bromovirus life cycle, emphasizing their temporal and spatial patterns during virus multiplication.Our knowledge of viral infection at the individual cell level determines our understanding of the infection at the entire plant body level. The idea of applying single-cell systems in virology was introduced with the first attempts to transfect Escherichia coli cells with a T4 anti-E. coli bacteriophage (27). E. C. Cocking was the first (1960) to enzymatically isolate plant cells (19), which were then infected with Tobacco mosaic tobamovirus (TMV) (20). The ensuing pioneer work showed that the infection was synchronous and that the uptake of viral particles/RNAs by protoplasts was efficient enough to support virus replication (5, 118). The first viral infection of protoplasts involved the use of poly-L-ornithine (5), but the trials that followed exploited the fusogenic polymers (24), liposomes (28), or electroporation (78,129). By 1980, these procedures had been successfully employed to transfect protoplasts from more than six species of plants, including various members of the Bromoviridae family, e.g., Brome mosaic bromovirus (BMV; 80), Cucumber mosaic cucumovirus (CMV; 69), and Cowpea chlorotic mottle virus (CCMV; 130). The first attempts were based on the transfection of plant cells with whole-virus particles (104). Later on, viral RNA and its chemical modifications were used as the inoculum (62). Further advances in nucleic acid technology, especially the accessibility of infectious transcripts, have broadened the application of protoplast systems to the study of Bromoviridae.The Bromoviridae constitute one of the most important families of plant RNA viruses. They are distributed worldwide, they infect an extensive range of hosts, and some of them (e.g., CMV and Broad bean mottle bromovirus) are responsible for major crop epidemics (111, 63). The family consists of five genera named after their most representative members: Alfamovirus, Bromovirus, Cucumovirus, Ilarvirus, and Oleavirus. All these viruses possess tripartite, single-stranded, positive-sense RNA genomes (Fig. 1). RNA1 and RNA2 encode the RNAdependent RNA polymerase (RdRp) proteins 1a and 2a, respectively. The dicistronic RNA3 encodes the movement protein (MP) and coat protein (CP). The latter is translated from subgenomic RNA 4 (sgRNA4). Many of the family members, such as CMV, BMV, and Alfalfa mosaic alfamovirus (AMV), repres...

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“…The effect of the plant host on accumulation of D-RNAs has been well documented (Hillman et al, 1987;Graves et al, 1996;Inoue-Nagata et al, 1998;Kaplan et al, 2004). Further, we have recently demonstrated that the host can affect the size of defective RNAs (Llamas et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Analysis of external factors that affect formation and accumulation of D-RNAs in Bromovirus infections

Sandoval

Llamas

Romero³

2008

Span. j. agric. res.

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Defective RNA molecules (D-RNAs) are being studied in several plant RNA virus groups. In the genus Bromovirus, D-RNAs have been described for Broad bean mottle virus (BBMV), they are formed by a single internal deletion in the RNA2 and have been generated de novo by serial passages. In contrast, in Brome mosaic virus (BMV) D-RNAs are generated by a single or double internal deletion in the RNA3 without serial passages in their hosts. In this work the external effects of the host and the growth temperature in the generation and accumulation of D-RNAs in BBMV, BMV and Cowpea chlorotic mottle virus (CCMV) are studied. The BBMV and BMV D-RNAs were generated and accumulated with or without serial passages of the viruses in different hosts and cultivars. Plants grown at 12, 16, 20 and 24°C in a growth chamber and in a greenhouse (22 ± 5°C) generated D-RNAs after being inoculated with virusfree D-RNAs, with and without passages. The D-RNAs observed in BBMV and BMV presented some common characteristics: both were formed de novo after serial passages or without passages, their deletion borders had short repeated and palindrome sequences that favour recombination. In addition, growing inoculated plants at lower temperatures greatly facilitated the generation and accumulation of D-RNAs. The CCMV did not generate defective molecules in cowpea (Vigna unguiculata) and Nicotiana benthamiana plants after several serial passages or without passages. This is the first time that D-RNAs have been generated in BBMV without passages and BMV with serial passages.Additional key words: BBMV, BMV, CCMV, host effects, temperature conditions. Resumen Análisis de los factores externos que afectan a la formación y acumulación de los D-RNAs en infecciones de BromovirusLos RNAs defectivos (D-RNAs) están siendo estudiados en diversos virus RNA de plantas. En el género Bromovirus se han descrito D-RNAs en el virus del moteado del haba (BBMV), formados mediante una delección interna en el RNA2, que se generan de novo mediante pases seriados del virus sobre un nuevo huésped. En contraste, en el virus del mosaico del bromo (BMV), los D-RNAs se forman por una o dos delecciones en el RNA3 sin necesidad de pases en sus huéspedes. En este trabajo estudiamos algunos factores externos, como los huéspedes, las inoculaciones y las temperaturas de crecimiento en la generación y acumulación de D-RNAs en BBMV, BMV y en el virus del moteado clorótico de la carilla (CCMV). Los D-RNAs de BBMV y BMV fueron generados y acumulados mediante pases seriados y sin pases de los virus en diferentes huéspedes y cultivares. Plantas inoculadas con BBMV y BMV sin D-RNAs, mantenidas a 12, 16, 20 y 24°C en cámaras de crecimiento a temperatura constante o en un invernadero (22 ± 5°C), generaron D-RNAs con o sin pases sobre nuevos huéspedes. Los D-RNAs observados en ambos virus presentan algunas características en común: son formados de novo mediante pases seriados o purificados de hojas infectadas algunas semanas después de la inoculación; los bordes de la delección tie...

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Host-specific encapsidation of a defective RNA 3 of Cucumber mosaic virus

Cited by 11 publications

References 26 publications

Deciphering the Mechanism of Defective Interfering RNA (DI RNA) Biogenesis Reveals That a Viral Protein and the DI RNA Act Antagonistically in Virus Infection

Deciphering the Mechanism of Defective Interfering RNA (DI RNA) Biogenesis Reveals That a Viral Protein and the DI RNA Act Antagonistically in Virus Infection

Insights into the Single-Cell Reproduction Cycle of Members of the Family Bromoviridae : Lessons from the Use of Protoplast Systems

Analysis of external factors that affect formation and accumulation of D-RNAs in Bromovirus infections

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