Umbravirus-Encoded Proteins both Stabilize Heterologous Viral RNA and Mediate Its Systemic Movement in Some Plant Species

Ryabov, Eugene V.; Robinson, David J.; Taliansky, Michael

doi:10.1006/viro.2001.1078

Cited by 51 publications

(33 citation statements)

References 46 publications

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“…[75][76][77][78] This protein shows no similarity to any viral or non-viral proteins (with the exception of the corresponding proteins of other umbraviruses) and acts as a long-distance movement protein which can bind viral RNA to form filamentous RNP particles that protect the RNA from degradation. 76,77 These particles accumulate as inclusions in the cytosol and are also thought to shuttle through the phloem to distribute the viral genome throughout the plant. 76,78 In addition to the ORF3 protein localizing to cytoplasmic inclusions, it has also appeared to interact with nuclei and is preferentially targeted to nucleoli.…”

Section: Virus Infectionsmentioning

confidence: 99%

Cajal bodies and their role in plant stress and disease responses

et al. 2016

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Cajal bodies (CBs) are distinct sub-nuclear structures that are present in eukaryotic living cells and are often associated with the nucleolus. CBs play important roles in RNA metabolism and formation of RNPs involved in transcription, splicing, ribosome biogenesis, and telomere maintenance. Besides these primary roles, CBs appear to be involved in additional functions that may not be directly related to RNA metabolism and RNP biogenesis. In this review, we assess possible roles of plant CBs in RNA regulatory pathways such as nonsense-mediated mRNA decay and RNA silencing. We also summarize recent progress and discuss new non-canonical functions of plant CBs in responses to stress and disease. It is hypothesized that CBs can regulate these responses via their interaction with poly(ADP ribose)polymerase (PARP), which is known to play an important role in various physiological processes including responses to biotic and abiotic stresses. It is suggested that CBs and their components modify PARP activities and functions.

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Section: Virus Infectionsmentioning

confidence: 99%

Cajal bodies and their role in plant stress and disease responses

et al. 2016

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“…The requirement of a functional capsid protein (CP) for systemic movement is common but not universal, depending on specific virus-host interactions (e.g. Dalmay et al, 1992;McGeachy & Barker, 2000;Petty & Jackson, 1990;Ryabov et al, 2001), and for most viruses the precise form in which the virus is transported has not been determined. Phloem unloading in the sink organs also parallels photoassimilate unloading and proceeds basipetally in the developing leaf during the sink-to-source transition (Cheng et al, 2000;Leisner et al, 1992; Roberts et al, 1997; Santa Cruz et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Analysis of the systemic colonization of cucumber plants by Cucumber green mottle mosaic virus

Moreno

Thompson

García‐Arenal

2004

Journal of General Virology

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Systemic movement of Cucumber green mottle mosaic virus (CGMMV) in cucumber plants was shown to be from photoassimilate source to sink, thus indicating phloem transport. Nevertheless, CGMMV was not detected by immunocytochemical procedures in the intermediary cell-sieve element complex in inoculated cotyledons, where photoassimilate loading occurs. In stem internodes, CGMMV was first localized in the companion cells of the external phloem and subsequently in all tissues except the medulla, therefore suggesting leakage of the virus from, and reloading into, the transport phloem during systemic movement. In systemically infected sink leaves, CGMMV was simultaneously detected in the xylem and phloem. Interestingly, CGMMV accumulated to high levels in the differentiating tracheids of young leaves implying that the xylem could be involved in the systemic movement of CGMMV. This possibility was tested using plants in which cell death was induced in a portion of the stem by steam treatment. At 24 6C, steam treatment effectively prevented the systemic movement of CGMMV, even though viral RNA was detected in washes of the xylem above the steamed internode suggesting that xylem circulation occurred. At 29 6C, CGMMV systemically infected steam-treated cucumber plants, indicating that CGMMV can move systemically via the xylem. Xylem transport of CGMMV was, however, less efficient than phloem transport in terms of the time required for systemic infection and the percentage of plants infected. INTRODUCTIONSystemic transport through the vascular system is a crucial step in plant virus infection. Most plant viruses are thought to move systemically through the phloem in parallel with photoassimilate transport (reviewed by Haywood et al., 2002;Lucas & Wolf, 1999;Nelson & Van Bel, 1998;Oparka & Turgeon, 1999;Thompson & Schulz, 1999). Phloem transport includes the loading (entry) of the virus into the phloem at source tissues, its circulation in the transport phloem and its unloading (exit) from the phloem at the sink tissues. Photoassimilate loading occurs presumably in the minor veins of source organs (Nelson & Van Bel, 1998;Santa Cruz, 1999) and in the case of cucurbits is thought to follow a symplastic route involving the specialized intermediary cell-sieve element complex (Turgeon, 1996). Knowledge of phloem circulation of plant viruses is far from complete, yet it is known that it parallels photoassimilate flow (Leisner et al., 1992;Oparka & Turgeon, 1999). The requirement of a functional capsid protein (CP) for systemic movement is common but not universal, depending on specific virus-host interactions (e.g. Dalmay et al., 1992;McGeachy & Barker, 2000;Petty & Jackson, 1990;Ryabov et al., 2001), and for most viruses the precise form in which the virus is transported has not been determined. Phloem unloading in the sink organs also parallels photoassimilate unloading and proceeds basipetally in the developing leaf during the sink-to-source transition (Cheng et al., 2000;Leisner et al., 1992; Roberts et al., 1997; Santa Cruz e...

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“…Nevertheless, they accumulate and spread efficiently within the infected plant; their lack of a CP is compensated for by the ORF3 protein. This protein fulfils umbraviral functions that are normally provided by the CPs of other plant viruses, such as long-distance movement of viral RNA through the phloem (17,18).…”

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confidence: 99%

Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection

Kim¹,

MacFarlane²,

Калинина

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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151

174

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The nucleolus and specific nucleolar proteins are involved in the life cycles of some plant and animal viruses, but the functions of these proteins and of nucleolar trafficking in virus infections are largely unknown. The ORF3 protein of the plant virus, groundnut rosette virus (an umbravirus), has been shown to cycle through the nucleus, passing through Cajal bodies to the nucleolus and then exiting back into the cytoplasm. This journey is absolutely required for the formation of viral ribonucleoprotein particles (RNPs) that, themselves, are essential for the spread of the virus to noninoculated leaves of the shoot tip. Here, we show that these processes rely on the interaction of the ORF3 protein with fibrillarin, a major nucleolar protein. Silencing of the fibrillarin gene prevents longdistance movement of groundnut rosette virus but does not affect viral replication or cell-to-cell movement. Repressing fibrillarin production also localizes the ORF3 protein to multiple Cajal bodylike aggregates that fail to fuse with the nucleolus. Umbraviral ORF3 protein and fibrillarin interact in vitro and, when mixed with umbravirus RNA, form an RNP complex. This complex has a filamentous structure with some regular helical features, resembling the RNP complex formed in vivo during umbravirus infection. The filaments formed in vitro are infectious when inoculated to plants, and their infectivity is resistant to RNase. These results demonstrate previously undescribed functions for fibrillarin as an essential component of translocatable viral RNPs and may have implications for other plant and animal viruses that interact with the nucleolus.Cajal bodies ͉ plant virus movement ͉ ribonucleoprotein particles T he nucleolus is a subnuclear domain and is the site of transcription and processing of rRNA and of ribosome biogenesis. In addition, the nucleolus also participates in other aspects of RNA metabolism and cell function (1, 2). The nucleolus is structurally and functionally associated with Cajal bodies (CBs), which are structures found in both animals and plants (3, 4). CBs contain different proteins including coilin, a protein essential for CB formation, and fibrillarin, a major nucleolar protein that is a core component of small nucleolar ribonucleoprotein particles (snoRNPs) and is required for rRNA processing (4-7). CBs are involved in the maturation of small nuclear RNPs (snRNPs) and snoRNPs, which traffic through CBs before accumulating in splicing speckles and the nucleolus, respectively (8, 9). Both the nucleolus and CBs have a role in RNA silencing in plants (10,11). Finally, a number of animal and plant viruses including the RNAcontaining tobacco etch virus and the DNA-containing tomato yellow leaf curl virus have a nucleolar phase in their life cycle (12, 13). Recently, we have shown that the ability of the umbravirus, groundnut rosette virus (GRV), to move long distances through the phloem, the specialized vascular system used by plants for the transport of assimilates and macromolecules, depends strictly on the...

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Umbravirus-Encoded Proteins both Stabilize Heterologous Viral RNA and Mediate Its Systemic Movement in Some Plant Species

Cited by 51 publications

References 46 publications

Cajal bodies and their role in plant stress and disease responses

Cajal bodies and their role in plant stress and disease responses

Analysis of the systemic colonization of cucumber plants by Cucumber green mottle mosaic virus

Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection

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