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Interaction of a Plant Virus-Encoded Protein with the Major Nucleolar Protein Fibrillarin Is Required for Systemic Virus Infection

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Interaction of a Plant Virus-Encoded Protein with the Major Nucleolar Protein Fibrillarin Is Required for Systemic Virus Infection Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection Sang Hyon Kim†, Stuart MacFarlane†, Natalia O. Kalinina†‡, Daria V. Rakitina†‡, Eugene V. Ryabov§, Trudi Gillespie†, Sophie Haupt†, John W. S. Brown†, and Michael Taliansky†¶ †Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, United Kingdom; ‡A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow 119992, Russia; and §Horticulture Research International, University of Warwick, Wellesbourne, Warwick CV35 9EF, United Kingdom Communicated by Bryan D. Harrison, Scottish Crop Research Institute, Dundee, United Kingdom, May 17, 2007 (received for review April 4, 2007) The nucleolus and specific nucleolar proteins are involved in the life Umbraviruses have RNA genomes and differ from most other cycles of some plant and animal viruses, but the functions of these viruses in that they do not encode a coat protein (CP) and so do not proteins and of nucleolar trafficking in virus infections are largely produce conventional virus particles in infected plants (15, 16). unknown. The ORF3 protein of the plant virus, groundnut rosette Nevertheless, they accumulate and spread efficiently within the virus (an umbravirus), has been shown to cycle through the infected plant; their lack of a CP is compensated for by the ORF3 nucleus, passing through Cajal bodies to the nucleolus and then protein. This protein fulfils umbraviral functions that are normally exiting back into the cytoplasm. This journey is absolutely required provided by the CPs of other plant viruses, such as long-distance for the formation of viral ribonucleoprotein particles (RNPs) that, movement of viral RNA through the phloem (17, 18). themselves, are essential for the spread of the virus to noninocu- The GRV ORF3 protein interacts with viral RNA in vivo to form lated leaves of the shoot tip. Here, we show that these processes filamentous RNP particles, which have elements of a regular helical rely on the interaction of the ORF3 protein with fibrillarin, a major structure but not the uniformity typical of virus particles (16). The nucleolar protein. Silencing of the fibrillarin gene prevents long- RNPs accumulate in cytoplasmic inclusions that are the form in distance movement of groundnut rosette virus but does not affect which the virus is thought to move through the phloem to cause viral replication or cell-to-cell movement. Repressing fibrillarin systemic infection (16). In addition to its presence in the cytoplasm, production also localizes the ORF3 protein to multiple Cajal body- the ORF3 protein is able to traffic into the nucleus, predominantly like aggregates that fail to fuse with the nucleolus. Umbraviral targeting the nucleolus (19, 20). The presence of the ORF3 protein ORF3 protein and fibrillarin interact in vitro and, when mixed with in the nucleolus was unexpected, because the entire infection cycle umbravirus RNA, form an RNP complex. This complex has a fila- of GRV and other umbraviruses was previously considered to be mentous structure with some regular helical features, resembling restricted to the cytoplasm. ORF3 proteins contain two conserved the RNP complex formed in vivo during umbravirus infection. The domains: an arginine-rich sequence (positions 108–122; R-rich filaments formed in vitro are infectious when inoculated to plants, domain) and a leucine-rich region (amino acids 148–156; L-rich PLANT BIOLOGY and their infectivity is resistant to RNase. These results demon- domain) (Fig. 1) (16, 20). The R-rich domain is involved in nuclear strate previously undescribed functions for fibrillarin as an essen- import, and the L149 residue, in addition to the R-rich domain, is tial component of translocatable viral RNPs and may have impli- essential for nucleolar targeting of the ORF3 protein (14, 20). The cations for other plant and animal viruses that interact with the whole L-rich region also acts as a nuclear export signal (20), nucleolus. suggesting that the ORF3 protein traffics between the nucleus (nucleolus) and cytoplasm of infected cells. Cajal bodies ͉ plant virus movement ͉ ribonucleoprotein particles The ORF3 protein is produced in the cytoplasm, enters the nucleus, and is targeted to CBs. The CBs are then reorganized into he nucleolus is a subnuclear domain and is the site of transcrip- multiple smaller structures (CB-like aggregates, CBLs) that move Ttion and processing of rRNA and of ribosome biogenesis. In to and fuse with the nucleolus by an unknown mechanism (14). The addition, the nucleolus also participates in other aspects of RNA ORF3 protein is exported from the nucleus, leading to the forma- metabolism and cell function (1, 2). The nucleolus is structurally tion of cytoplasmic viral RNP particles that are transported to the and functionally associated with Cajal bodies (CBs), which are rest of the plant via the phloem. The integral connection between structures found in both animals and plants (3, 4). CBs contain nucleolar targeting of the ORF3 protein and its biological function different proteins including coilin, a protein essential for CB in virus long-distance spread has been demonstrated by the intro- formation, and fibrillarin, a major nucleolar protein that is a core duction of mutations in the R- and L-rich domains that block component of small nucleolar ribonucleoprotein particles nucleolar localization and nuclear export of the ORF3 protein, (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 splic- Author contributions: S.H.K., S.M., N.O.K., J.W.S.B., and M.T. designed research; S.H.K., ing speckles and the nucleolus, respectively (8, 9). Both the nucle- S.M., D.V.R., E.V.R., T.G., and S.H. performed research; S.H.K., N.O.K., D.V.R., J.W.S.B., and M.T. analyzed data; and S.H.K., J.W.S.B., and M.T. wrote the paper. olus and CBs have a role in RNA silencing in plants (10, 11). Finally, The authors declare no conflict of interest. a number of animal and plant viruses including the RNA- Abbreviations: CB, Cajal bodies; CBL, CB-like aggregates; GRV, groundnut rosette virus; containing tobacco etch virus and the DNA-containing tomato TMV, tobacco mosaic virus; PVX, potato virus X; TRV, tobacco rattle virus; RNP, ribonucle- yellow leaf curl virus have a nucleolar phase in their life cycle (12, oprotein; Fib2, fibrillarin 2; GAR, glycine- and arginine-rich domain; CP, coat protein. 13). Recently, we have shown that the ability of the umbravirus, Data deposition: The nucleotide sequence of the NbFib cDNA was deposited in GenBank groundnut rosette virus (GRV), to move long distances through the (accession no. AM269909). phloem, the specialized vascular system used by plants for the ¶To whom correspondence should be addressed. E-mail: [email protected]. transport of assimilates and macromolecules, depends strictly on This article contains supporting information online at www.pnas.org/cgi/content/full/ the interaction of one of its proteins, the ORF3 protein, with CBs 0704632104/DC1. and the nucleolus (14). © 2007 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0704632104 PNAS ͉ June 26, 2007 ͉ vol. 104 ͉ no. 26 ͉ 11115–11120 Downloaded by guest on September 28, 2021 Fig. 1. Correlation between the ability of the ORF3 protein to traffic through the nucleolus and the relocalization of fibrillarin, formation of viral RNPs, and long-distance movement. Wild-type and mutant ORF3 protein sequences of the R-rich and L–rich domains are shown in combination with data on nuclear (N) and nucleolar (No) localization, nuclear export (N-exp) of the ORF3 pro- tein, relocalization of fibrillarin (Cyt. fibrillarin), RNP formation, and virus long-distance movement (LDM) (14). respectively, resulting in failure to form viral RNPs, and of their long-distance movement (14) (Fig. 1). In elucidating the nuclear pathway of the ORF3 protein, we also observed the partial relocalization of the nucleolar protein, fibril- larin, to the cytoplasmic inclusions containing viral RNPs, whereas normally, fibrillarin does not accumulate in cytoplasm (14). Fibril- larin is one of the major proteins of the nucleolus. It is also localized to CBs, is a core component of box C/D snoRNPs, and has Fig. 2. Virus-induced silencing of the fibrillarin gene (NbFib) in N. benthami- methyltransferase activity directing methylation of rRNA and snR- ana plants by using a TRV vector. (A–C) Expression of fibrillarin was suppressed NAs (21). Interaction of some animal viruses with fibrillarin and by TRV-NbFib to different levels, and plants with effectively three different other nucleolar proteins has been reported (12, 13, 22, 23), but their phenotypes (I, II, and III) were generated. (A) Growth phenotypes of silenced specific role in virus infections remains elusive. In this article, we plants in comparison with control (c) nonsilenced plants. (B) Semiquantitative demonstrate a previously uncharacterized function of fibrillarin in RT-PCR analysis of NbFib mRNA accumulation. Ethidium bromide-stained umbravirus systemic infection. The GRV ORF3 protein directly agarose gels show RT-PCR products corresponding to the fragments of NbFib interacts with fibrillarin, and this interaction is essential for nucle- (Fib) mRNA (320 bp) and ubiquitin mRNA (176 bp) used as a control, as indicated by arrows. Lanes 1–3 represent plant replicates. (C) Western blot olar localization of the ORF3 protein. Fibrillarin is also required, analysis of fibrillarin (Fib) accumulation. The position of fibrillarin is shown by along with umbravirus ORF3 protein and viral RNA, for the an arrow. Lanes 1–3 as above. (D) Immunofluorescence staining of cells of assembly of movement-competent, infectious RNP particles. Thus, fibrillarin-silenced (group II; Fib-s) and nonsilenced (Non-s) plants with fibril- the ORF3 protein may exploit fibrillarin trafficking to reach the larin and coilin antibodies visualized by confocal microscopy.
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