Plant Virus RNA Replication


Plant RNA (ribonucleic acid) viruses are obligate intracellular parasites with single‐stranded (ss) or double‐stranded RNA genome(s) generally encapsidated but rarely enveloped. For viruses with ssRNA genomes, the polarity of the infectious RNA (positive or negative) and the presence of one or more genomic RNA segments are the features that mostly determine the molecular mechanisms governing the replication process. RNA viruses cannot penetrate plant cell walls unaided and must enter the cellular cytoplasm through mechanically induced wounds or assisted by a biological vector. After desencapsidation, their genome remains in the cytoplasm where it is translated, replicated and encapsidated in a coupled manner. Replication occurs in large viral replication complexes (VRCs), tethered to modified membranes of cellular organelles and composed by the viral RNA templates and by viral and host proteins. Cis‐acting elements located in viral RNA templates regulate the recognition by the virus‐encoded RNA‐dependent RNA polymerase and possibly contribute to VRC assembly and/or activation.

Key Concepts

  • The vast majority of plant RNA viruses have positive (mRNA sense) single‐stranded RNA genome.
  • Some plant RNA viruses have negative single‐stranded, or double‐stranded RNA genome.
  • Replication is at the core of the infection cycle of plant RNA viruses and occurs solely through RNA intermediates of positive and negative polarities.
  • Replication of most plant RNA viruses takes place in viral replication complexes tethered to modified membranes of cytoplasmic organelles.
  • Viral replication complexes are dynamic and contain the viral RNA, viral replication proteins and proteins from the host.
  • A viral‐RNA‐dependent RNA polymerase is responsible for the synthesis of new genomic RNA using parental genome as template.
  • Viral proteins and co‐opted host factors orchestrate the targeting of the genomic RNA to the membranes where replication takes place; they also contribute to the remodelling of the membranes that are used as scaffolds for tethering the viral replication complexes.
  • In addition to the role of co‐opted host factors in controlling the biogenesis of replication organelles and the composition, assembly and/or activity of the viral replication complex, they can post‐translationally modify viral proteins to regulate replication.
  • Primary sequence and structure elements of viral RNAs regulate template selection, initiation of the synthesis of complementary RNA strands and the assembly and activation of viral replication complexes.

Keywords: plant; RNA; virus; replication; host factor; RNA‐dependent RNA polymerase; cis‐acting; viral replication complex

Figure 1. Cellular life cycles of plant RNA viruses. For each class of RNA virus, a simplified and representative life cycle is shown. All three virus classes replicate exclusively through RNA intermediates in the cytoplasm. Nuclear trafficking of macromolecules during viral replication could not be ruled out. Virions are shown as black hexagons containing positive (+) and/or negative (−) RNA strands in red and green, respectively, and viral‐RNA‐dependent RNA polymerase (RdRp, blue circle). Other viral proteins are shown as filled circles of distinct colours. (a) Life cycle of (+) RNA viruses. The genomic RNA (gRNA) from virions is released into the cytoplasm. This (+) RNA, mRNA sense, is translated to produce several viral proteins including the viral RdRp. This polymerase copies the (+) strands into (−) strands that serve as templates for the synthesis of (+) strands that can be translated, replicated or assembled in virion particles. (b) Life cycle of the majority of (−) RNA viruses. The gRNA is used as a template by the viral RdRp to generate (+) strand mRNAs that are released into the cytoplasm to be translated into viral proteins. The gRNA is also copied into full‐length (+) strands that, in turn, serve as templates for (−) RNA synthesis. For members of the genus Nucleorhabdovirus, replication occurs in the nucleus. (c) Life cycle of double‐stranded RNA (dsRNA) viruses. Viral RdRp synthesises and releases into the cytoplasm (+) strands that are first translated and then packaged to form immature virions. Virions mature by synthesising (−) RNA and by the addition of other viral proteins.
Figure 2. Cis‐acting RNA elements in viral genomic RNAs (gRNAs) involved in genome replication. A diagram corresponding to the linear RNA genome is shown for each selected virus described in the main text. RNA elements in the viral RNA genome involved in replication are shown in orange, and the long‐range interactions between them are shown in blue dotted lines. (a) RNA elements in Tomato bushy stunt virus (TBSV) gRNA. (b) RNA elements in Red clover necrotic mosaic virus (RCNMV) gRNAs. (c) RNA elements in Brome mosaic virus (BMV) gRNAs. Adapted from Newburn and White © Elsevier.


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Further Reading

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Saxena P and Lomonossoff GP (2014) Virus infection cycle events coupled to RNA replication. Annual Review of Phytopathology 52: 197–212.

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Carbonell, Alberto, García, Juan Antonio, Simón‐Mateo, Carmen, and Hernández, Carmen(Jul 2016) Plant Virus RNA Replication. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0022338]