Nina I. Lukhovitskaya

University of Cambridge

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Eugene I. Savenkov

Swedish University of Agricultural Sciences

Andrew E. Firth

University of Cambridge

Andrey G. Solovyev

Lomonosov Moscow State University

Sergey Y. Morozov

Lomonosov Moscow State University

L. Torrance

James Hutton Institute

Graham H. Cowan

James Hutton Institute

Ingrida Olendraitė

Addenbrooke's Hospital

Ramesh R. Vetukuri

Swedish University of Agricultural Sciences

Hazel Stewart

University of Cambridge

Srinivas Thaduri

Swedish University of Agricultural Sciences

Cooperative Institutions

University of Cambridge

Swedish University of Agricultural Sciences

Lomonosov Moscow State University

Centre National de la Recherche Scientifique

Addenbrooke's Hospital

Université de Strasbourg

James Hutton Institute

Institut de Biologie Moléculaire des Plantes

Wageningen University & Research

Crop Research Institute

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Interaction of the Carlavirus Cysteine-Rich Protein with the Plant Defense System

Molecular Biology (2005)

Nina I. Lukhovitskaya Andrey G. Solovyev T. E. Koshkina С. К. Завриев Sergey Y. Morozov

Potato virus X

Agroinfiltration

10.1007/s11008-005-0094-9

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Citations (10)

Role of the zinc-finger and basic motifs of chrysanthemum virus B p12 protein in nucleic acid binding, protein localization and induction of a hypersensitive response upon expression from a viral vector

Journal of General Virology (2009)

Nina I. Lukhovitskaya Igor V. Ignatovich Eugene I. Savenkov Joachim Schiemann Sergey Y. Morozov

The genomes of carlaviruses encode cysteine-rich proteins (CRPs) of unknown function. The 12 kDa CRP of chrysanthemum virus B (CVB), p12, has been shown previously to induce a hypersensitive response (HR) when expressed from potato virus X (PVX). This study demonstrated that a p12-induced HR was preceded by induction of a number of genes related to pathogenesis, stress and systemic acquired resistance. p12 localized predominantly to the nucleus. Interestingly, it was found that p12 bound both RNA and DNA in vitro, but notably exhibited a preference for DNA in the presence of Zn(2+) ions. Mutational analysis of the p12 conserved sequence motifs demonstrated that the basic motif is required for p12 translocation to the nucleus, thus representing part of the protein nuclear localization signal, whereas the predicted zinc finger motif is needed for both Zn(2+)-dependent DNA binding and eliciting an HR in PVX-infected leaves. Collectively, these results link, for the first time, nuclear localization of the protein encoded by a cytoplasmically replicating virus and its DNA-binding capacity with HR induction. Furthermore, these data suggest that p12 may mediate induction of the host genes by binding to the plant genomic DNA, and emphasize that CVB p12 is functionally distinct from other known nuclear-localized proteins encoded by the plant positive-stranded RNA viruses.

Potato virus X

10.1099/vir.0.005025-0

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Citations (32)

Expression, localization and effects on virulence of the cysteine-rich 8 kDa protein of Potato mop-top virus

Journal of General Virology (2005)

Nina I. Lukhovitskaya Nataliya E. Yelina Andrey A. Zamyatnin Mikhail Schepetilnikov Andrey G. Solovyev

Potato mop-top virus (PMTV) RNA3 contains a triple gene block (TGB) encoding viral movement proteins and an open reading frame for a putative 8 kDa cysteine-rich protein (CRP). In this study, PMTV CRP was shown to be expressed in the course of virus infection, and a PMTV CRP-specific subgenomic RNA was mapped. CRP has previously been shown to be dispensable for infection of PMTV in Nicotiana benthamiana. In this study, PMTV CRP was found to increase the severity of disease symptoms when expressed from Potato virus X or Tobacco mosaic virus in N. benthamiana and Nicotiana tabacum, suggesting that the protein affects virulence of the virus or might suppress a host defence mechanism. However, PMTV CRP did not show RNA silencing suppression activity in three assays. Host responses to the PMTV CRP expression from different viral genomes ranged from an absence of response to extreme resistance at a single cell level and were dependent on the viral genome. These findings emphasized involvement of viral proteins and/or virus-induced cell components in the plant reaction to CRP. PMTV CRP was predicted to possess a transmembrane segment. CRP fused to the green fluorescent protein was associated with endoplasmic reticulum-derived membranes and induced dramatic rearrangements of the endoplasmic reticulum structure, which might account for protein functions as a virulence factor of the virus.

Infectivity

10.1099/vir.0.81099-0

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High-scale analysis of pathogenicity determinants of Potato mop-top virus

BMC Plant Biology (2005)

Andrey A. Zamyatnin Natasha Yelina Nina I. Lukhovitskaya Andrey G. Solovyev Anna Germundsson

Background: At their natural environment plants are exposed to high fluxes of photosynthetically active and UV radiation.The increased synthesis of UV-absorbing compounds, such as flavonoids and other polyphenols, are accepted as a plant response to increased UV radiation.The increase of leaf flavonoid content can be a protection against the harmful effect of UV-B radiation as they function as antioxidant and UV filters in plants.Differences between sun and shade leaves (adapted to high light and low light respectively) of some tree species are analysed, taking in consideration differences on the UV-A absorption via fluorescence imaging of leaves.Materials and methods: Leaves of beech (Fagus sylvatica L.), maple (Platanus hybrida L.) and poplar (Populus nigra L.) were analysed.The Karlsruhe flash-lamp fluorescence imaging system (FL-FIS) was used to measure images at the fluorescence bands blue, green, red and far-red.The decline of chlorophyll fluorescence from Fp to the steady-state Fs was imaged too [1].Results: Shade leaves exhibited a much higher chlorophyll fluorescence yield than sun leaves.Also differences in the distribution of the fluorescence over the whole leaf were detected which are due to the lower chlorophyll content of shade leaves and a lower reabsorption of the emitted F690 band.Shade leaves are characterized by lower values of the fluorescence ratios blue/red (F440/F690) and blue/far-red (F440/F740) than sun leaves.Both ratios are early indicators of stress to the photosynthetic apparatus.The fluorescence ratio red/far-red expressed lower values in sun leaves and is an indicator of their higher chlorophyll content (curvilinear inverse correlation).The R Fd -images (R Fd = (Fp-Fs)/Fs) as indicators of photosynthetic activity allow to evaluate differences in photosynthetic quantum conversion.Conclusion: The observed differences in the fluorescence images and chlorophyll fluorescence images allow to characterize the different properties of sun and shade leaves related to their adaptation to high light and high UV-radiation or low light and low UV-radiation.

Tobamovirus

Infectivity

Agroinfiltration

10.1186/1471-2229-5-s1-s39

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Making sense of nuclear localization: A zinc-finger protein encoded by a cytoplasmically replicating plant RNA virus acts a transcription factor

Plant Signaling & Behavior (2013)

Nina I. Lukhovitskaya Vladimir А. Gushchin Andrey G. Solovyev Eugene I. Savenkov

Recent studies have uncovered numerous nucleus-localized proteins encoded by plant RNA viruses. Whereas for some of these viruses nuclear (or, more specifically, nucleolar) passage of the proteins is needed for the virus movement within the plant or suppression of host defense, the nuclear function of these proteins remains largely unknown. Recently, the situation has been clarified for one group of plant RNA viruses, the Carlaviruses. Being positive-stranded RNA viruses, carlaviruses multiply exclusively in the cytoplasm. Chrysanthemum virus B (CVB, a carlavirus) encodes a zinc-finger protein p12 targeted to the nucleus in a nuclear localization signal-dependent manner. In a recent work, we demonstrated that p12 directly interacts with chromatin and plant promoters, thus, acts as a eukaryotic transcription factor (TF) and activates expression of a host TF involved in regulation of cell size and proliferation to favor virus infection. Therefore our studies identified a novel nuclear stage of in CVB infection involving modulation of host gene expression and plant development. Whereas it is well established that any RNA virus actively replicating in the cell causes changes in the transcriptome, our study expanded this view by showing that some positive-stranded RNA viruses can directly manipulate host transcription by encoding eukaryotic TFs.

Transcription

RNA virus

10.4161/psb.25263

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Discovery of three RNA viruses using ant transcriptomic datasets

Archives of Virology (2018)

Eleni Kleanthous Ingrida Olendraitė Nina I. Lukhovitskaya Andrew E. Firth

Three novel RNA viruses, named Formica fusca virus 1 (GenBank accession no. MH477287), Lasius neglectus virus 2 (MH477288) and Myrmica scabrinodis virus 2 (MH477289), were discovered in ants collected in Cambridge, UK. The proposed virus names were given based on the hosts in which they were identified. The genome sequences were obtained using de novo transcriptome assembly of high-throughput RNA sequencing reads and confirmed by Sanger sequencing. Phylogenetic analysis showed that Formica fusca virus 1 grouped within the family Nyamiviridae, Lasius neglectus virus 2 grouped within the family Rhabdoviridae and Myrmica scabrinodis virus 2 belongs to the family Dicistroviridae. All three viruses are highly divergent from previously sequenced viruses.

RNA virus

Sanger sequencing

Lasius

Virus classification

RNA-Seq

10.1007/s00705-018-4093-2

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Unusual Long-Distance Movement Strategies of Potato mop-top virus RNAs in Nicotiana benthamiana

Molecular Plant-Microbe Interactions (2009)

L. Torrance Nina I. Lukhovitskaya Mikhail Schepetilnikov Graham H. Cowan Angelika Ziegler

The Potato mop-top virus (PMTV) genome encodes replicase, movement, and capsid proteins on three different RNA species that are encapsidated within tubular rod-shaped particles. Previously, we showed that the protein produced on translational readthrough (RT) of the coat protein (CP) gene, CP-RT, is associated with one extremity of the virus particles, and that the two RNAs encoding replicase and movement proteins can move long distance in the absence of the third RNA (RNA-CP) that encodes the capsid proteins, CP and CP-RT. Here, we examined the roles of the CP and CP-RT proteins on RNA movement using infectious clones carrying mutations in the CP and CP-RT coding domains. The results showed that, in infections established with mutant RNA-CP expressing CP together with truncated CP-RT, systemic movement of the mutant RNA-CP was inhibited but not the movement of the other two RNAs. Furthermore, RNA-CP long-distance movement was inhibited in a mutant clone expressing only CP in the absence of the CP-RT polypeptide. CP-RT was not necessary for particle assembly because virions were observed in leaf extracts infected with the CP-RT deletion mutants. RNA-CP moved long distance when protein expression was suppressed completely or when CP expression was suppressed so that only CP-RT or truncated CP-RT was expressed. CP-RT but not CP interacted with the movement protein TGB1 in the yeast two-hybrid system. CP-RT and TGB1 were detected by enzyme-linked immunosorbent assay in virus particles and the long-distance movement of RNA-CP was correlated with expression of CP-RT that interacted with TGB1; mutant RNA-CP expressing truncated CP-RT proteins that did not interact with TGB1 formed virions but did not move to upper noninoculated leaves. The results indicate that PMTV RNA-CP can move long distance in two distinct forms: either as a viral ribonucleoprotein complex or as particles that are most likely associated with CP-RT and TGB1.

Movement protein

10.1094/mpmi-22-4-0381

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Citations (33)

Polycipiviridae: a proposed new family of polycistronic picorna-like RNA viruses

Journal of General Virology (2017)

Ingrida Olendraitė Nina I. Lukhovitskaya Sanford D. Porter Steven M. Valles Andrew E. Firth

Solenopsis invicta virus 2 is a single-stranded positive-sense picorna-like RNA virus with an unusual genome structure. The monopartite genome of approximately 11 kb contains four open reading frames in its 5′ third, three of which encode proteins with homology to picornavirus-like jelly-roll fold capsid proteins. These are followed by an intergenic region, and then a single long open reading frame that covers the 3′ two-thirds of the genome. The polypeptide translation of this 3′ open reading frame contains motifs characteristic of picornavirus-like helicase, protease and RNA-dependent RNA polymerase domains. An inspection of public transcriptome shotgun assembly sequences revealed five related apparently nearly complete virus genomes isolated from ant species and one from a dipteran insect. By high-throughput sequencing and in silico assembly of RNA isolated from Solenopsis invicta and four other ant species, followed by targeted Sanger sequencing, we obtained nearly complete genomes for four further viruses in the group. Four further sequences were obtained from a recent large-scale invertebrate virus study. The 15 sequences are highly divergent (pairwise amino acid identities of as low as 17 % in the non-structural polyprotein), but possess the same overall polycistronic genome structure, which is distinct from all other characterized picorna-like viruses. Consequently, we propose the formation of a new virus family, Polycipiviridae, to classify this clade of arthropod-infecting polycistronic picorna-like viruses. We further propose that this family be divided into three genera: Chipolycivirus (2 species), Hupolycivirus (2 species) and Sopolycivirus (11 species), with members of the latter infecting ants in at least 3 different subfamilies.

Picornavirus

RNA virus

Intergenic region

10.1099/jgv.0.000902

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Citations (38)

Cauliflower mosaic virus transactivator protein (TAV) can suppress nonsense-mediated decay by targeting VARICOSE, a scaffold protein of the decapping complex

Scientific Reports (2019)

Nina I. Lukhovitskaya Lyubov A. Ryabova

Abstract During pathogenesis, viruses hijack the host cellular machinery to access molecules and sub-cellular structures needed for infection. We have evidence that the multifunctional viral translation transactivator/viroplasmin (TAV) protein from Cauliflower mosaic virus (CaMV) can function as a suppressor of nonsense-mediated mRNA decay (NMD). TAV interacts specifically with a scaffold protein of the decapping complex VARICOSE (VCS) in the yeast two-hybrid system, and co-localizes with components of the decapping complex in planta. Notably, plants transgenic for TAV accumulate endogenous NMD-elicited mRNAs, while decay of AU-rich instability element (ARE)-signal containing mRNAs are not affected. Using an agroinfiltration-based transient assay we confirmed that TAV specifically stabilizes mRNA containing a premature termination codon (PTC) in a VCS-dependent manner. We have identified a TAV motif consisting of 12 of the 520 amino acids in the full-length sequence that is critical for both VCS binding and the NMD suppression effect. Our data suggest that TAV can intercept NMD by targeting the decapping machinery through the scaffold protein VARICOSE, indicating that 5′-3′ mRNA decapping is a late step in NMD-related mRNA degradation in plants.

Cauliflower mosaic virus

Nonsense-Mediated Decay

Brome mosaic virus

10.1038/s41598-019-43414-0

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Citations (22)

The N-Terminal Domain of PMTV TGB1 Movement Protein Is Required for Nucleolar Localization, Microtubule Association, and Long-Distance Movement

Molecular Plant-Microbe Interactions (2010)

Kathryn M. Wright Graham H. Cowan Nina I. Lukhovitskaya Jens Tilsner Alison G. Roberts

The triple-gene-block (TGB)1 protein of Potato mop-top virus (PMTV) was fused to fluorescent proteins and expressed in epidermal cells of Nicotiana benthamiana under the control of the 35S promoter. TGB1 fluorescence was observed in the cytoplasm, nucleus, and nucleolus and occasionally associated with microtubules. When expressed from a modified virus (PMTV.YFP-TGB1) which formed local lesions but was not competent for systemic movement, yellow fluorescent protein (YFP)-TGB1 labeled plasmodesmata in cells at the leading edge of the lesion and plasmodesmata, microtubules, nuclei, and nucleoli in cells immediately behind the leading edge. Deletion of 84 amino acids from the N-terminus of unlabeled TGB1 within the PMTV genome abolished movement of viral RNA to noninoculated leaves. When the same deletion was introduced into PMTV.YFP-TGB1, labeling of microtubules and nucleoli was abolished. The N-terminal 84 amino acids of TGB1 were fused to green fluorescent protein (GFP) and expressed in epidermal cells where GFP localized strongly to the nucleolus (not seen with unfused GFP), indicating that these amino acids contain a nucleolar localization signal; the fusion protein did not label microtubules. This is the first report of nucleolar and microtubule association of a TGB movement protein. The results suggest that PMTV TGB1 requires interaction with nuclear components and, possibly, microtubules for long-distance movement of viral RNA.

Movement protein

Plasmodesma

Bimolecular fluorescence complementation

10.1094/mpmi-05-10-0105

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Citations (58)