Similarities in intracellular transport of plant viral movement proteins BMB2 and TGB3

Lazareva, Ekaterina A.; Lezzhov, Alexander A.; Golyshev, Sergey A.; Morozov, Sergey Y.; Heinlein, Manfred; Solovyev, Andrey G.

doi:10.1099/jgv.0.000914

Cited by 9 publications

(14 citation statements)

References 59 publications

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“…The constructs for the transient expression of BMB1, BMB2 and its N‐ and C‐terminal fusions to fluorescent proteins, ST‐GFP, ER‐GFP, ER‐monomeric red fluorescent protein (mRFP), PVX‐POL‐GFP (Lazareva et al ., 2017a,b), VAP27‐mRFP (Atabekova et al ., 2018), as well as constructs YN, YC, YN‐ER and YC‐ER used for membrane protein topology studies (Zamyatnin Jr. et al ., 2006), were described previously. To obtain binary vectors carrying PVX TGB2 and TGB3 genes, the respective fragments from constructs pRT‐12K and pRT‐8K (Solovyev et al ., 2000) were subcloned into pLH* (Solovyev et al ., 2013).…”

Section: Methodsmentioning

confidence: 99%

“…thaliana Derlin1 (Der1) (Lee et al, 2013), an integral ER protein with four transmembrane segments and with its N-and Ctermini presumably located in the cytoplasm (Katiyar et al, 2005). Expression of Der1 fused to GFP at its C-terminus (Der1-GFP) together with luminal ER-mRFP marker (Lazareva et al, 2017a) led to overlapping patterns of red and green fluorescence, highlighting the normal structure of the cortical ER network ( Fig. 2a-c) in agreement with the previously described localization of A. thaliana Derlin1 to the ER membranes (Katiyar et al, 2005).…”

Section: New Phytologistmentioning

confidence: 99%

“…Moreover, BMB2 recruits diffuse cytosolic BMB1 to these membrane bodies and to PD, and enables BMB1 spread to neighboring cells (Lazareva et al ., 2017b). The intracellular transport of BMB2 to PD‐associated sites is independent of the ER–Golgi secretory pathway but requires a functional ER/actin network (Lazareva et al ., 2017a). However, the ER/actin‐associated mechanism by which BMB2 facilitates transport to and through PD is not known.…”

Section: Introductionmentioning

confidence: 99%

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Reticulon‐like properties of a plant virus‐encoded movement protein

et al. 2020

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Plant viruses encode movement proteins (MPs) that ensure the transport of viral genomes through plasmodesmata (PD) and use cell endomembranes, mostly the endoplasmic reticulum (ER), for delivery of viral genomes to PD and formation of PD-anchored virus replication compartments. Here, we demonstrate that the Hibiscus green spot virus BMB2 MP, an integral ER protein, induces constrictions of ER tubules, decreases the mobility of ER luminal content, and exhibits an affinity to highly curved membranes. These properties are similar to those described for reticulons, cellular proteins that induce membrane curvature to shape the ER tubules. Similar to reticulons, BMB2 adopts a W-like topology within the ER membrane. BMB2 targets PD and increases their size exclusion limit, and these BMB2 activities correlate with the ability to induce constrictions of ER tubules. We propose that the induction of ER constrictions contributes to the BMB2-dependent increase in PD permeability and formation of the PD-associated replication compartments, therefore facilitating the virus intercellular spread. Furthermore, we show that the ER tubule constrictions also occur in cells expressing TGB2, one of the three MPs of Potato virus X (PVX), and in PVX-infected cells, suggesting that reticulon-like MPs are employed by diverse RNA viruses.

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Section: Methodsmentioning

confidence: 99%

Section: New Phytologistmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Reticulon‐like properties of a plant virus‐encoded movement protein

et al. 2020

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“…BMB-like gene modules consisting of two genes were also identified in plant transcriptome RNA-seq data assembled into RNA virus-like contigs [virus-like RNA assemblies (VLRA)] ( Morozov and Solovyev, 2015 ). HGSV BMB1 and BMB2 were found to be necessary and sufficient to mediate viral cell-to-cell movement ( Lazareva et al, 2017b ), and further studies revealed similarities in mechanisms of intracellular transport of BMB and TGB proteins ( Lazareva et al, 2017a ). Taking into account a distant relationship of TGB and BMB proteins, we hypothesize that the BMB transport module could represent an evolutionary snapshot of intermediate stage of TGB evolution corresponding to the TGB1/TGB2 genomic block.…”

Section: Origin and Functional Significance Of Small Membrane Proteinmentioning

confidence: 99%

Non-replicative Integral Membrane Proteins Encoded by Plant Alpha-Like Viruses: Emergence of Diverse Orphan ORFs and Movement Protein Genes

Solovyev

Morozov

2017

Front. Plant Sci.

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Fast accumulation of sequencing data on plant virus genomes and plant transcriptomes demands periodic re-evaluation of current views on the genome evolution of viruses. Here, we substantiate and further detail our previously mostly speculative model on the origin and evolution of triple gene block (TGB) encoding plant virus movement proteins TGB1, TGB2, and TGB3. Recent experimental data on functional competence of transport gene modules consisting of two proteins related to TGB1 and TGB2, as well as sequence analysis data on similarity of TGB2 and TGB3 encoded by a viral genome and virus-like RNAs identified in a plant transcriptomes, suggest that TGB evolution involved events of gene duplication and gene transfer between viruses. In addition, our analysis identified that plant RNA-seq data assembled into RNA virus-like contigs encode a significant variety of hydrophobic proteins. Functions of these orphan proteins are still obscure; however, some of them are obviously related to hydrophobic virion proteins of recently sequenced invertebrate (mostly insect) viruses, therefore supporting the current view on a common origin for many groups of plant and insect RNA-containing viruses. Moreover, these findings may suggest that the function of at least some orphan hydrophobic proteins is to provide plant viruses with the ability to infect insect hosts. In general, our observations emphasize that comparison of RNA virus sequences in a large variety of land plants and algae isolated geographically and ecologically may lead to experimental confirmation of previously purely speculative schemes of evolution of single genes, gene modules, and whole genomes.

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“…Moreover, BMB2 directs BMB1, having helicase activity, to the membrane bodies, to the Pd interior cavity and to neighboring cells [58] . The BMB2 intracellular transport to Pd-associated sites does not involve the secretory pathway, but requires the functional ER/actin network [168] .…”

Section: Binary Movement Blockmentioning

confidence: 99%

Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes

Morozov

Solovyev

2020

AIMS Microbiology

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Most plant viruses code for movement proteins (MPs) targeting plasmodesmata to enable cell-to-cell and systemic spread in infected plants. Small membrane-embedded MPs have been first identified in two viral transport gene modules, triple gene block (TGB) coding for an RNA-binding helicase TGB1 and two small hydrophobic proteins TGB2 and TGB3 and double gene block (DGB) encoding two small polypeptides representing an RNA-binding protein and a membrane protein. These findings indicated that movement gene modules composed of two or more cistrons may encode the nucleic acid-binding protein and at least one membrane-bound movement protein. The same rule was revealed for small DNA-containing plant viruses, namely, viruses belonging to genus Mastrevirus (family Geminiviridae ) and the family Nanoviridae . In multi-component transport modules the nucleic acid-binding MP can be viral capsid protein(s), as in RNA-containing viruses of the families Closteroviridae and Potyviridae . However, membrane proteins are always found among MPs of these multicomponent viral transport systems. Moreover, it was found that small membrane MPs encoded by many viruses can be involved in coupling viral replication and cell-to-cell movement. Currently, the studies of evolutionary origin and functioning of small membrane MPs is regarded as an important pre-requisite for understanding of the evolution of the existing plant virus transport systems. This paper represents the first comprehensive review which describes the whole diversity of small membrane MPs and presents the current views on their role in plant virus movement.

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Similarities in intracellular transport of plant viral movement proteins BMB2 and TGB3

Cited by 9 publications

References 59 publications

Reticulon‐like properties of a plant virus‐encoded movement protein

Reticulon‐like properties of a plant virus‐encoded movement protein

Non-replicative Integral Membrane Proteins Encoded by Plant Alpha-Like Viruses: Emergence of Diverse Orphan ORFs and Movement Protein Genes

Small hydrophobic viral proteins involved in intercellular movement of diverse plant virus genomes

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