Bromoviridae : A Family of Plant Viruses with Tripartite Genomes

Abstract

The family Bromoviridae contains six genera of tripartite, plant‐pathogenic ribonucleic acid (RNA) viruses, namely Alfamovirus, Anulavirus, Bromovirus, Cucumovirus, Ilarvirus and Oleavirus . Viruses in this family exhibit the following salient features: (1) virions are nonenveloped with icosahedral or bacilliform geometries; (2) in each genus, the single‐strand, positive‐sense RNA genome of ∼8 kilobases (kb) is divided among three RNAs; (3) the 3' untranslated region of the viral RNAs adopts either a transfer ribonucleic acid‐like structure (TLS) or a series of stem loops that assume a TLS upon coat protein (CP) binding; (4) four progeny RNAs are packaged into either three homogeneous or four heterogeneous virions; (5) CP is required for the genome activation exclusively for Alfamovirus and Ilarvirus genera; (6) in all the genera, the replication and virion assembly occurs in the cytoplasmic compartment of the cell and (7) cell‐to‐cell and long‐distance spread involves both movement protein and CP. Finally, members of Bromoviridae and other plant viruses commonly share mechanical and insect transmission properties. Key Concepts The genome of the member viruses of the family Bromoviridae contains single‐strand, positive‐sense RNAs encoding few proteins. A group of three RNA components represents the genome in tripartite viruses. Vesicles or spherule‐like invaginations of host membranes induced by virus‐encoded gene products are the sites of viral replication. Progeny RNA of tripartite viruses is packaged into three or four virions having either spherical or bacilliform morphology. Genome packaging into stable virions requires specific interaction between the coat protein (CP) and the viral progeny RNA and is functionally coupled to replication, that is only the replicated progeny RNA is packaged into virions. Cell‐to‐cell spread of the tripartite viruses requires both movement protein and CP.

The diversity of protein-protein interaction interfaces within T=3 icosahedral viral capsids

“…An additional role of the capsid flexibly could be to allow it to package genomes of slightly varying sizes. Unlike Tymoviridae and Tombusviridae , viruses belonging to Bromoviridae have their genome divided in four parts that are packaged separately in three different capsids (tripartite genomes) ( Chaturvedi and Rao, 2018 ; Chakravarty and Rao, 2021 ). It was also shown that the C-terminal tail which forms the dimerization interface in Bromoviridae may be important for cell-to-cell movement of the viral capsids ( Okinaka et al, 2001 ).…”

Modulation of Capsid Dynamics in Bromoviruses by the Host and Heterologous Viral Replicase

“…In bromoviruses, gene products encoded by RNA3 play essential roles in replication and host adaptability (22). In CCMV and BMV, CP mRNA production depends on the replication of the genomic RNA3 (4, 23). Following translation, CP stimulates the asymmetric synthesis of the plus-strand over the minus strand (24), and its interaction with replicase dictates packaging specificity (25).…”

“…Following entry and initial replication in primary cells, all plant viruses must spread to the neighboring cells (i.e., cell-to-cell movement) via plasmodesmata with the help of a dedicated and virus-encoded MP (27). However, in BMV and CCMV, both MP and CP are obligatory for cell-to-cell spread (4). A majority of plant viruses, including bromoviruses, manifesting the long-distance spread require assembled virions.…”

“…The three single-stranded, positive-sense genomic RNA molecules of the two closely related members of the family Bromoviridae, namely Cowpea chlorotic mottle virus (CCMV; C1, C2, and C3) and Brome mosaic virus (BMV; B1, B2, and B3) are encapsidated separately into three individual virions (4). The two largest monocistronic genomic RNAs of CCMV and BMV-RNA1 (C1, 3171 nt and B1, 3237 nt) and- RNA2 (C2, 2774 nt and B2, 2864 nt), encoding nonstructural replicase proteins 1a (methyltransferase/helicase-like) and 2a (RNA-dependent RNA polymerase) respectively, are packaged separately into two virion types, C1 V /B1 V and C2 V /B2 V (4). The dicistronic genomic RNA3 (C3 and B3) encodes a nonstructural movement protein (MP) at its 5’ and a structural CP at its 3’ end.…”

“…The CPs of CCMV and BMV are 190 and 189 amino acids in length (aa), respectively, and are 70% homologous. In these two viruses, the first N-terminal 25 aa region of the CP is not visible in the crystal structure since this highly basic region projects into the interior region interacting with the RNA, while the remainder of the CP is highly structured (4). The interaction between amino and carboxyl termini is essential for forming CP dimers, the building blocks for the virus assembly (12).…”