Partitivirus Structure Reveals a 120-Subunit, Helix-Rich Capsid with Distinctive Surface Arches Formed by Quasisymmetric Coat-Protein Dimers

Ochoa, Wendy F.; Havens, Wendy M.; Sinkovits, Robert S.; Nibert, Max L.; Ghabrial, Said A.; Baker, Timothy S.

doi:10.1016/j.str.2008.02.014

Cited by 59 publications

(65 citation statements)

References 47 publications

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“…Even in capsids with a smaller triangulation number, such as the T ϭ 7 capsid observed by heterologous expression of selected IBDV proteins (11), space would be sufficient to accommodate a single genome copy. Furthermore, fungal viruses with multipartite dsRNA genomes, such as chrysovirus (25) and partitivirus (26), package each dsRNA segment in separate particles rather than in a single capsid. This feature is also described for comovirus, a group of plant viruses with a genome consisting of 2 molecules of positive-strand ssRNA (27).…”

Section: Discussionmentioning

confidence: 99%

Infectious bursal disease virus is an icosahedral polyploid dsRNA virus

Luque¹,

Rivas

Alfonso

et al. 2009

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

117

102

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Viruses are a paradigm of the economy of genome resources, reflected in their multiplication strategy and for their own structure. Although there is enormous structural diversity, the viral genome is always enclosed within a proteinaceous coat, and most virus species are haploid; the only exception to this rule are the highly pleomorphic enveloped viruses. We performed an in-depth characterization of infectious bursal disease virus (IBDV), a nonenveloped icosahedral dsRNA virus with a bisegmented genome. Up to 6 natural populations can be purified, which share a similar protein composition but show higher sedimentation coefficients as particle density increases. Stoichiometry analysis of their genome indicated that these biophysical differences correlate with the copy number of dsRNA segments inside the viral capsid. This is a demonstration of a functional polyploid icosahedral dsRNA virus. We show that IBDV particles with greater genome copy number have higher infectivity rates. Our results show an unprecedented replicative strategy for dsRNA viruses and suggest that birnaviruses are living viral entities encompassing numerous functional and structural characteristics of positive and negative ssRNA viruses.cargo volume ͉ IBDV ͉ icosahedral dsRNA viruses ͉ life cycle ͉ viral polyploidy

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Section: Discussionmentioning

confidence: 99%

Infectious bursal disease virus is an icosahedral polyploid dsRNA virus

Luque¹,

Rivas

Alfonso

et al. 2009

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

117

102

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“…Whereas there are numerous functional and structural studies of the family Reoviridae, it is clear that deeper characterization of many fungal and protozoal dsRNA viruses is needed. Recent studies of fungal viruses of the family Partitiviridae identified the first Tϭ1 capsid formed by quasisymmetric CP dimers (48,49); an equivalent structure in viruses in higher eukaryotes, the picobirnaviruses, was also recently described (18). Another notable example is infectious myonecrosis virus (IMNV), a shrimp pathogen with a totivirus-like 120-subunit capsid.…”

Section: Discussionmentioning

confidence: 99%

“…These capsids are an extended feature of dsRNA viruses (Fig. 1); they are described (i) in members of the family Reoviridae (37,44,69,71), which infect mostly higher eukaryotic systems, (ii) in viruses of the family Picobirnaviridae (18), a recently established taxonomic family whose members infect humans and other vertebrates, (iii) in bacteriophages of the family Cystoviridae, which infect the prokaryote Pseudomonas syringae (26,28), (iv) and in viruses of the families Totiviridae (12,13,67) and Partitiviridae (48), which mostly infect unicellular and simple eukaryotes (fungi and protozoa). A notable exception is the Penicillium chrysogenum virus (PcV) of the family Chrysoviridae, which has an authentic Tϭ1 capsid formed by just 60 copies of one polypeptide (11).…”

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confidence: 99%

The T=1 Capsid Protein of Penicillium chrysogenum Virus Is Formed by a Repeated Helix-Rich Core Indicative of Gene Duplication

Luque

González

Garriga

et al. 2010

J Virol

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Penicillium chrysogenum virus (PcV), a member of the Chrysoviridae family, is a double-stranded RNA (dsRNA) fungal virus with a multipartite genome, with each RNA molecule encapsidated in a separate particle. Chrysoviruses lack an extracellular route and are transmitted during sporogenesis and cell fusion. The PcV capsid, based on a T‫1؍‬ lattice containing 60 subunits of the 982-amino-acid capsid protein, remains structurally undisturbed throughout the viral cycle, participates in genome metabolism, and isolates the virus genome from host defense mechanisms. Using three-dimensional cryoelectron microscopy, we determined the structure of the PcV virion at 8.0 Å resolution. The capsid protein has a high content of rod-like densities characteristic of ␣-helices, forming a repeated ␣-helical core indicative of gene duplication. Whereas the PcV capsid protein has two motifs with the same fold, most dsRNA virus capsid subunits consist of dimers of a single protein with similar folds. The spatial arrangement of the ␣-helical core resembles that found in the capsid protein of the L-A virus, a fungal totivirus with an undivided genome, suggesting a conserved basic fold. The encapsidated genome is organized in concentric shells; whereas the inner dsRNA shells are well defined, the outermost layer is dense due to numerous interactions with the inner capsid surface, specifically, six interacting areas per monomer. The outermost genome layer is arranged in an icosahedral cage, sufficiently well ordered to allow for modeling of an A-form dsRNA. The genome ordering might constitute a framework for dsRNA transcription at the capsid interior and/or have a structural role for capsid stability.Viruses with double-stranded RNA (dsRNA) genomes are found in a broad range of organisms, ranging from bacteria to simple (fungi and protozoa) and complex (animals and plants) eukaryotes.

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“…Small aliquots (2 to 3 l) of purified SsPV1 virions were vitrified, and cryo-EM image data were recorded essentially as described previously for the partitivirus Penicillium stoloniferum virus S (PsV-S) (25). A total of 23 micrographs were recorded at 200 keV under low-dose conditions (ϳ15 e/Å 2 ) at underfocus settings ranging between 3.8 and 11 m on a Gatan Ultrascan 4K 2 charge-coupled-device (CCD) camera with an FEI Polara Tecnai microscope at a nominal magnification of ϫ76,900 (yielding an effective pixel size of 1.8 Å).…”

Section: Methodsmentioning

confidence: 99%

“…A system in which partitivirus particles (i.e., Rosellinia necatrix partitivirus 1-W8 [RnPV1-W8]) can be transfected into fungal protoplasts has been successfully established and was utilized to confirm that RnPV1-W8 has a broad host range in Sordariomycetes (23,24). Particle structures determined by cryo-electron microscopy (cryo-EM) and three-dimensional (3D) image reconstruction, as well as one determined by X-ray crystallography, have shown three different partitivirus capsids to have a so-called "Tϭ2" organization comprising 60 capsid protein (CP) dimers arranged on a Tϭ1 icosahedral lattice (25)(26)(27). These developments and technological advances have facilitated research on different aspects of the biology of fungal partitiviruses, such as virus-host interactions, virion structure, virus evolution, and host range.…”

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confidence: 99%

A Novel Partitivirus That Confers Hypovirulence on Plant Pathogenic Fungi

Xiao

Chéng

Tang

et al. 2014

J Virol

Self Cite

131

103

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Members of the family Partitiviridae have bisegmented double-stranded RNA (dsRNA) genomes and are not generally known to cause obvious symptoms in their natural hosts. An unusual partitivirus, Sclerotinia sclerotiorum partitivirus 1 (SsPV1/WF-1), conferred hypovirulence on its natural plant-pathogenic fungal host, Sclerotinia sclerotiorum strain WF-1. Cellular organelles, including mitochondria, were severely damaged. Hypovirulence and associated traits of strain WF-1 and SsPV1/WF-1 were readily cotransmitted horizontally via hyphal contact to different vegetative compatibility groups of S. sclerotiorum and interspecifically to Sclerotinia nivalis and Sclerotinia minor. S. sclerotiorum strain 1980 transfected with purified SsPV1/WF-1 virions also exhibited hypovirulence and associated traits similar to those of strain WF-1. Moreover, introduction of purified SsPV1/WF-1 virions into strain KY-1 of Botrytis cinerea also resulted in reductions in virulence and mycelial growth and, unexpectedly, enhanced conidial production. However, virus infection suppressed hyphal growth of most germinating conidia of B. cinerea and was eventually lethal to infected hyphae, since very few new colonies could develop following germ tube formation. Taken together, our results support the conclusion that SsPV1/WF-1 causes hypovirulence in Sclerotinia spp. and B. cinerea. Cryo-EM (cryo-electron microscopy) reconstruction of the SsPV1 particle shows that it has a distinct structure with similarity to the closely related partitiviruses Fusarium poae virus 1 and Penicillium stoloniferum virus F. These findings provide new insights into partitivirus biological activities and clues about molecular interactions between partitiviruses and their hosts. IMPORTANCEMembers of the Partitiviridae are believed to occur commonly in their phytopathogenic fungal and plant hosts. However, most partitiviruses examined so far appear to be associated with latent infections. Here we report a partitivirus, SsPV1/WF-1, that was isolated from a hypovirulent strain of Sclerotinia sclerotiorum and describe its biological and molecular features. We have demonstrated that SsPV1 confers hypovirulence. Furthermore, SsPV1 can infect and cause hypovirulence in Botrytis cinerea. Our study also suggests that SsPV1 has a vigorous ability to proliferate and spread via hyphal contact. SsPV1 can overcome vegetative incompatibility barriers and can be transmitted horizontally among different vegetative compatibility groups of S. sclerotiorum, even interspecifically. Cryo-EM reconstruction of SsPV1 shows that it has a distinct structure with similarity to closely related partitiviruses. Our studies exploit a novel system, SsPV1 and its hosts, which can provide the means to explore the mechanisms by which partitiviruses interact with their hosts.

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Partitivirus Structure Reveals a 120-Subunit, Helix-Rich Capsid with Distinctive Surface Arches Formed by Quasisymmetric Coat-Protein Dimers

Cited by 59 publications

References 47 publications

Infectious bursal disease virus is an icosahedral polyploid dsRNA virus

Infectious bursal disease virus is an icosahedral polyploid dsRNA virus

The T=1 Capsid Protein of Penicillium chrysogenum Virus Is Formed by a Repeated Helix-Rich Core Indicative of Gene Duplication

A Novel Partitivirus That Confers Hypovirulence on Plant Pathogenic Fungi

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