A novel block of plant virus movement genes

Abstract

Hibiscus green spot virus (HGSV) is a recently discovered and so far poorly characterized bacilliform plant virus with a positive-stranded RNA genome consisting of three RNA species. Here, we demonstrate that the proteins encoded by the ORF2 and ORF3 in HGSV RNA2 are necessary and sufficient to mediate cell-to-cell movement of transport-deficient Potato virus X in Nicotiana benthamiana. These two genes represent a specialized transport module called a 'binary movement block' (BMB), and ORF2 and ORF3 are termed BMB1 and BMB2 genes. In agroinfiltrated epidermal cells of N. benthamiana, green fluorescent protein (GFP)-BMB1 fusion protein was distributed diffusely in the cytoplasm and the nucleus. However, in the presence of BMB2, GFP-BMB1 was directed to cell wall-adjacent elongated bodies at the cell periphery, to cell wall-embedded punctate structures co-localizing with callose deposits at plasmodesmata, and to cells adjacent to the initially transformed cell. Thus, BMB2 can mediate the transport of BMB1 to and through plasmodesmata. In general, our observations support the idea that cell-to-cell trafficking of movement proteins involves an initial delivery to membrane compartments adjacent to plasmodesmata, subsequent entry of the plasmodesmata cavity and, finally, transport to adjacent cells. This process, as an alternative to tubule-based transport, has most likely evolved independently in triple gene block (TGB), double gene block (DGB), BMB and the single gene-coded transport system.

A novel insect-infecting virga/nege-like virus group and its pervasive endogenization into insect genomes

“…Thus, it is suggested that acquisition of a gene(s) responsible for viral movement might be essential for certain insect viruses to fully adapt to the plant hosts. It is possible that this event(s) occurred during the course of evolution of cile/higrevirus and blunevirus lineages (Lazareva et al, 2017) (Fig. S1).…”

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

“…In the course of adaptation to various hosts, viruses with potex-like TGB might have acquired host-specific dependence of cell-to-cell movement on the type of their VRC. However, our recent experimental data on HGSV BMB indicate that the distant relatives of TGB1 and TGB2 encoded by HGSV – BMB1 and BMB2 – are, rather efficiently, able to support movement of TGB-deficient PVX, although HGSV BMB1 and BMB2, apparently, do not have obvious adaptation to PVX VRC ( Lazareva et al, 2017b ). Thus, if the need of a tight connection of VRC to movement is not essential for virus multiplication and spread, some viruses like CsVX and CsNAV can move cell-to-cell in their natural hosts using only the activities of TGB1 and TGB2.…”

“…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.…”

“…BNRBV RNA4 contains a single ORF coding for 3a-like MP, whereas RNA3 codes for two “orphan” hydrophobic polypeptides SP24 and p31 ( Quito-Avila et al, 2013 ). HGSV RNA2 encodes recently experimentally characterized BMB MPs, and RNA3 codes for SP24 and “orphan” hydrophobic proteins p33 and p29 ( Melzer et al, 2012 ; Kuchibhatla et al, 2014 ; Lazareva et al, 2017b ).…”

Silicon and Nitrate Differentially Modulate the Symbiotic Performances of Healthy and Virus-Infected Bradyrhizobium-nodulated Cowpea (Vigna unguiculata), Yardlong Bean (V. unguiculata subsp. sesquipedalis) and Mung Bean (V. radiata)

“…The typical symptoms of CCMV or CMMV infections were evident in all CCMV- or CMMV-infected N 2 fixing plants of the three Vigna taxa, although, in terms of growth and nodulation, CMMV proved to be more virulent than CCMV in cowpea and yardlong bean plants. It is known that carlaviruses replicate and assemble in the cytoplasm of infected cells [ 78 ], with encoded cysteine-rich proteins being the determinants of pathogenicity [ 79 ], and the coat proteins being essential for cell-to-cell movement and long-distance transport [ 80 ]. In contrast, bromoviruses replicate and assemble in the cytoplasm associated with the endoplasmic reticulum [ 81 , 82 ], and the cell-to-cell movement and long-distance transport of virions are dependent on a non-structural movement protein encoded by the dicistronic genomic RNA3, but independent of the capsid [ 83 ].…”