A plant virus movement protein forms ringlike, complexes with the major nucleolar protein, fibrillarin, in vitro

Elisabetta Canetta, Sang Hyon Kim, Natalia O. Kalinina, Jane Shaw, Ashok K. Adya, Trudi Gillespie, John W. S. Brown, Michael Taliansky

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Fibrillarin, one of the major proteins of the nucleolus, has methyltransferase activity directing 2′-O-ribose methylation of rRNA and snRNAs and is required for rRNA processing. The ability of the plant umbravirus, groundnut rosette virus, to move long distances through the phloem, the specialized plant vascular system, has been shown to strictly depend on the interaction of one of its proteins, the ORF3 protein (protein encoded by open reading frame 3), with fibrillarin. This interaction is essential for several stages in the groundnut rosette virus life cycle such as nucleolar import of the ORF3 protein via Cajal bodies, relocalization of some fibrillarin from the nucleolus to cytoplasm, and assembly of cytoplasmic umbraviral ribonucleoprotein particles that are themselves required for the long-distance spread of the virus and systemic infection. Here, using atomic force microscopy, we determine the architecture of these complexes as singlelayered ringlike structures with a diameter of 18–22 nm and a height of 2.0±0.4 nm, which consist of several (n=6–8) distinct protein granules. We also estimate the molar ratio of fibrillarin to ORF3 protein in the complexes as approximately 1:1. Based on these data, we propose a model of the structural organization of fibrillarin–ORF3 protein complexes and discuss potential mechanistic and functional implications that may also apply to other viruses.
Original languageEnglish
Pages (from-to)932-937
Number of pages6
JournalJournal of Molecular Biology
Volume376
Issue number4
DOIs
Publication statusPublished - 29 Feb 2008

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Plant Viral Movement Proteins
Nuclear Proteins
Proteins
Viruses
Phloem
Ribonucleoproteins
Ribose
In Vitro Techniques
fibrillarin
Atomic Force Microscopy
Structural Models
Methyltransferases
Virus Diseases
Life Cycle Stages
Methylation
Open Reading Frames
Blood Vessels
Cytoplasm

Cite this

Canetta, E., Kim, S. H., Kalinina, N. O., Shaw, J., Adya, A. K., Gillespie, T., ... Taliansky, M. (2008). A plant virus movement protein forms ringlike, complexes with the major nucleolar protein, fibrillarin, in vitro. Journal of Molecular Biology, 376(4), 932-937. https://doi.org/10.1016/j.jmb.2007.12.039
Canetta, Elisabetta ; Kim, Sang Hyon ; Kalinina, Natalia O. ; Shaw, Jane ; Adya, Ashok K. ; Gillespie, Trudi ; Brown, John W. S. ; Taliansky, Michael. / A plant virus movement protein forms ringlike, complexes with the major nucleolar protein, fibrillarin, in vitro. In: Journal of Molecular Biology. 2008 ; Vol. 376, No. 4. pp. 932-937.
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Canetta, E, Kim, SH, Kalinina, NO, Shaw, J, Adya, AK, Gillespie, T, Brown, JWS & Taliansky, M 2008, 'A plant virus movement protein forms ringlike, complexes with the major nucleolar protein, fibrillarin, in vitro', Journal of Molecular Biology, vol. 376, no. 4, pp. 932-937. https://doi.org/10.1016/j.jmb.2007.12.039

A plant virus movement protein forms ringlike, complexes with the major nucleolar protein, fibrillarin, in vitro. / Canetta, Elisabetta; Kim, Sang Hyon; Kalinina, Natalia O.; Shaw, Jane; Adya, Ashok K.; Gillespie, Trudi; Brown, John W. S.; Taliansky, Michael.

In: Journal of Molecular Biology, Vol. 376, No. 4, 29.02.2008, p. 932-937.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A plant virus movement protein forms ringlike, complexes with the major nucleolar protein, fibrillarin, in vitro

AU - Canetta, Elisabetta

AU - Kim, Sang Hyon

AU - Kalinina, Natalia O.

AU - Shaw, Jane

AU - Adya, Ashok K.

AU - Gillespie, Trudi

AU - Brown, John W. S.

AU - Taliansky, Michael

PY - 2008/2/29

Y1 - 2008/2/29

N2 - Fibrillarin, one of the major proteins of the nucleolus, has methyltransferase activity directing 2′-O-ribose methylation of rRNA and snRNAs and is required for rRNA processing. The ability of the plant umbravirus, groundnut rosette virus, to move long distances through the phloem, the specialized plant vascular system, has been shown to strictly depend on the interaction of one of its proteins, the ORF3 protein (protein encoded by open reading frame 3), with fibrillarin. This interaction is essential for several stages in the groundnut rosette virus life cycle such as nucleolar import of the ORF3 protein via Cajal bodies, relocalization of some fibrillarin from the nucleolus to cytoplasm, and assembly of cytoplasmic umbraviral ribonucleoprotein particles that are themselves required for the long-distance spread of the virus and systemic infection. Here, using atomic force microscopy, we determine the architecture of these complexes as singlelayered ringlike structures with a diameter of 18–22 nm and a height of 2.0±0.4 nm, which consist of several (n=6–8) distinct protein granules. We also estimate the molar ratio of fibrillarin to ORF3 protein in the complexes as approximately 1:1. Based on these data, we propose a model of the structural organization of fibrillarin–ORF3 protein complexes and discuss potential mechanistic and functional implications that may also apply to other viruses.

AB - Fibrillarin, one of the major proteins of the nucleolus, has methyltransferase activity directing 2′-O-ribose methylation of rRNA and snRNAs and is required for rRNA processing. The ability of the plant umbravirus, groundnut rosette virus, to move long distances through the phloem, the specialized plant vascular system, has been shown to strictly depend on the interaction of one of its proteins, the ORF3 protein (protein encoded by open reading frame 3), with fibrillarin. This interaction is essential for several stages in the groundnut rosette virus life cycle such as nucleolar import of the ORF3 protein via Cajal bodies, relocalization of some fibrillarin from the nucleolus to cytoplasm, and assembly of cytoplasmic umbraviral ribonucleoprotein particles that are themselves required for the long-distance spread of the virus and systemic infection. Here, using atomic force microscopy, we determine the architecture of these complexes as singlelayered ringlike structures with a diameter of 18–22 nm and a height of 2.0±0.4 nm, which consist of several (n=6–8) distinct protein granules. We also estimate the molar ratio of fibrillarin to ORF3 protein in the complexes as approximately 1:1. Based on these data, we propose a model of the structural organization of fibrillarin–ORF3 protein complexes and discuss potential mechanistic and functional implications that may also apply to other viruses.

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DO - 10.1016/j.jmb.2007.12.039

M3 - Article

VL - 376

SP - 932

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JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

SN - 0022-2836

IS - 4

ER -