Plant viral proteins and fibrillarin: the link to complete the infective cycle

Decle-Carrasco, Stefano; Rodríguez-Zapata, Luis Carlos; Castaño, Enrique

doi:10.1007/s11033-021-06401-1

Cited by 8 publications

(5 citation statements)

References 98 publications

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“…To our knowledge, none of these RBPs have previously been shown to play a role in facilitating alphavirus replication, or for the most part, other RNA viruses. Interestingly, FBL is well described to play a role in movement of plant viruses (reviewed in [44]) and has also been implicated in enhancing translation of structural genes of some viruses (reviewed in [45]). The mechanism of enhanced translation has been proposed to be mediated through protein-protein interactions, thus how FBL enhances enzootic VEEV replication through RNA interactions remains to be determined.…”

Section: Discussionmentioning

confidence: 99%

RNA structures within Venezuelan equine encephalitis virus E1 alter macrophage replication fitness and contribute to viral emergence

Hickson,

Hyde

2024

Preprint

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Venezuelan equine encephalitis virus (VEEV) is a mosquito-borne +ssRNA virus belonging to theTogaviridae. VEEV is found throughout Central and South America and is responsible for periodic epidemic/epizootic outbreaks of febrile and encephalitic disease in equines and humans. Endemic/enzootic VEEV is transmitted between Culex mosquitoes and sylvatic rodents, whereas epidemic/epizootic VEEV is transmitted between mosquitoes and equids, which serve as amplification hosts during outbreaks. Epizootic VEEV emergence has been shown to arise from mutation of enzootic VEEV strains. Specifically, epizootic VEEV has been shown to acquire amino acid mutations in the E2 viral glycoprotein that facilitate viral entry and equine amplification. However, the abundance of synonymous mutations which accumulate across the epizootic VEEV genome suggests that other viral determinants such as RNA secondary structure may also play a role in VEEV emergence. In this study we identify novel RNA structures in the E1 gene which specifically alter replication fitness of epizootic VEEV in macrophages but not other cell types. We show that SNPs are conserved within epizootic lineages and that RNA structures are conserved across different lineages. We also identified several novel RNA-binding proteins that are necessary for altered macrophage replication. These results suggest that emergence of VEEV in nature requires multiple mutations across the viral genome, some of which alter cell-type specific replication fitness in an RNA structure-dependent manner.AUTHOR SUMMARYUnderstanding how viral pathogens emerge is critical for ongoing surveillance and outbreak preparedness. However, our understanding of the molecular mechanisms that drive viral emergence are still not completely understood. Emergence of the mosquito-borne virus Venezuelan equine encephalitis virus (VEEV) is known to require mutations in the viral attachment protein (E2), which drive viremia and transmission. We have observed that emergent strains (epizootic VEEV) also accumulate many silent mutations, suggesting that other determinants independent of protein sequence also contributes to emergence. In this study we identify novel RNA secondary structures associated with epizootic VEEV that alters viral replication in a cell-type dependent manner. We show that these RNA structures are conserved across epizootic viruses and identify host proteins that specifically bind these RNAs. These findings imply that viral emergence requires multiple mutations, a number of which likely alter viral structure in a manner that benefits viral replication and transmission.

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Section: Discussionmentioning

confidence: 99%

RNA structures within Venezuelan equine encephalitis virus E1 alter macrophage replication fitness and contribute to viral emergence

Hickson,

Hyde

2024

Preprint

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“…The nucleolus, besides being the site of rRNA synthesis and ribosome biogenesis, is also implicated in gene silencing, stress responses, and many other aspects of plant cell functioning [ 42 ]. Fibrillarin has multiple functions in plant cell among which is the participation in cell-to-cell and long-distance movements of viruses [ 43 ]. Coilin and Cajal bodies are also implicated in the responses to biotic and abiotic stress factors and serve targets for viruses [ 36 , 44 ].…”

Section: Discussionmentioning

confidence: 99%

Nicotiana benthamiana Methanol-Inducible Gene (MIG) 21 Encodes a Nucleolus-Localized Protein That Stimulates Viral Intercellular Transport and Downregulates Nuclear Import

Sheshukova,

Kamarova,

Ershova

et al. 2024

Plants

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The mechanical damage of plant tissues leads to the activation of methanol production and its release into the atmosphere. The gaseous methanol or vapors emitted by the damaged plant induce resistance in neighboring intact plants to bacterial pathogens but create favorable conditions for viral infection spread. Among the Nicotiana benthamiana methanol-inducible genes (MIGs), most are associated with plant defense and intercellular transport. Here, we characterize NbMIG21, which encodes a 209 aa protein (NbMIG21p) that does not share any homology with annotated proteins. NbMIG21p was demonstrated to contain a nucleolus localization signal (NoLS). Colocalization studies with fibrillarin and coilin, nucleolus and Cajal body marker proteins, revealed that NbMIG21p is distributed among these subnuclear structures. Our results show that recombinant NbMIG21 possesses DNA-binding properties. Similar to a gaseous methanol effect, an increased NbMIG21 expression leads to downregulation of the nuclear import of proteins with nuclear localization signals (NLSs), as was demonstrated with the GFP-NLS model protein. Moreover, upregulated NbMIG21 expression facilitates tobacco mosaic virus (TMV) intercellular transport and reproduction. We identified an NbMIG21 promoter (PrMIG21) and showed that it is methanol sensitive; thus, the induction of NbMIG21 mRNA accumulation occurs at the level of transcription. Our findings suggest that methanol-activated NbMIG21 might participate in creating favorable conditions for viral reproduction and spread.

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“…Upon viral infection, it has been observed that host nucleolar proteins undergo redistribution to other cellular compartments or modifications, while non‐nucleolar cellular proteins are relocated to the nucleolus. A recent report has indicated that the interaction of animal viruses, including human viruses, triggers the redistribution of fibrillarin, the main nucleolar protein, to the nucleoplasm and cytoplasm, disrupting its role in pre‐rRNA processing (Decle‐Carrasco et al ., 2023). In plants, viruses sequester fibrillarin to complete their infective cycle by forming an efficiently mobile RNA complex with its assistance (Decle‐Carrasco et al ., 2021).…”

Section: Discussionmentioning

confidence: 99%

“…A recent report has indicated that the interaction of animal viruses, including human viruses, triggers the redistribution of fibrillarin, the main nucleolar protein, to the nucleoplasm and cytoplasm, disrupting its role in pre‐rRNA processing (Decle‐Carrasco et al ., 2023). In plants, viruses sequester fibrillarin to complete their infective cycle by forming an efficiently mobile RNA complex with its assistance (Decle‐Carrasco et al ., 2021). For example, the GRV‐encoded ORF3 protein induces CB‐like structures in the nucleolus through its interaction with fibrillarin, resulting in the formation of filamentous ribonucleoproteins (RNPs) that facilitate viral RNP trafficking and systemic invasion of the plant (Kim et al ., 2007a,b).…”

Section: Discussionmentioning

confidence: 99%

“…Various stresses, such as UV irradiation, heat shock, transcriptional inhibition, osmotic stress, starvation, and viral infections, can induce re‐arrangements of CBs, affecting their number, integrity, structure, and architecture (Boulon et al ., 2010). While the role of CBs in virus‐sensing mechanisms in mammalian cells has been extensively discussed (Decle‐Carrasco et al ., 2023), their functions in response to virus infections in plants are a newly identified area of study (Love et al ., 2017). Particularly intriguing is the interplay between CBs and viral infections, which is now recognized as a relevant aspect in multiple plant–virus interactions (Ding and Lozano‐Durán, 2020).…”

Section: Introductionmentioning

confidence: 99%

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A viral protein competitively bound to rice CIPK23 inhibits potassium absorption and facilitates virus systemic infection in rice

Jing,

Wang,

Liu

et al. 2024

Plant Biotechnology Journal

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SummaryPotassium (K+) plays a crucial role as a macronutrient in the growth and development of plants. Studies have definitely determined the vital roles of K+ in response to pathogen invasion. Our previous investigations revealed that rice plants infected with rice grassy stunt virus (RGSV) displayed a reduction in K+ content, but the mechanism by which RGSV infection subverts K+ uptake remains unknown. In this study, we found that overexpression of RGSV P1, a specific viral protein encoded by viral RNA1, results in enhanced sensitivity to low K+ stress and exhibits a significantly lower rate of K+ influx compared to wild‐type rice plants. Further investigation revealed that RGSV P1 interacts with OsCIPK23, an upstream regulator of Shaker K+ channel OsAKT1. Moreover, we found that the P1 protein recruits the OsCIPK23 to the Cajal bodies (CBs). In vivo assays demonstrated that the P1 protein competitively binds to OsCIPK23 with both OsCBL1 and OsAKT1. In the nucleus, the P1 protein enhances the binding of OsCIPK23 to OsCoilin, a homologue of the signature protein of CBs in Arabidopsis, and facilitates their trafficking through these CB structures. Genetic analysis indicates that mutant in oscipk23 suppresses RGSV systemic infection. Conversely, osakt1 mutants exhibited increased sensitivity to RGSV infection. These findings suggest that RGSV P1 hinders the absorption of K+ in rice plants by recruiting the OsCIPK23 to the CB structures. This process potentially promotes virus systemic infection but comes at the expense of inhibiting OsAKT1 activity.

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Plant viral proteins and fibrillarin: the link to complete the infective cycle

Cited by 8 publications

References 98 publications

RNA structures within Venezuelan equine encephalitis virus E1 alter macrophage replication fitness and contribute to viral emergence

RNA structures within Venezuelan equine encephalitis virus E1 alter macrophage replication fitness and contribute to viral emergence

Nicotiana benthamiana Methanol-Inducible Gene (MIG) 21 Encodes a Nucleolus-Localized Protein That Stimulates Viral Intercellular Transport and Downregulates Nuclear Import

A viral protein competitively bound to rice CIPK23 inhibits potassium absorption and facilitates virus systemic infection in rice

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