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. 2018 Nov 27:9:1776.
doi: 10.3389/fpls.2018.01776. eCollection 2018.

The Role of the Chloroplast in the Replication of Positive-Sense Single-Stranded Plant RNA Viruses

Marta Budziszewska  1 , Aleksandra Obrępalska-Stęplowska  1
Affiliations

The Role of the Chloroplast in the Replication of Positive-Sense Single-Stranded Plant RNA Viruses

Marta Budziszewska et al. Front Plant Sci. .

Abstract

Positive-sense single-stranded plant RNA viruses are obligate intracellular parasites that infect many agriculturally important crops. Most known plant RNA viruses are characterized by small genomes encoding a limited number of multifunctional viral proteins. Viral pathogens are considered to be absolutely dependent on their hosts, and viruses must recruit numerous host proteins and other factors for genomic RNA replication. Overall, the replication process depends on virus-plant protein-protein, RNA-protein and protein-lipid interactions. Recent publications provide strong evidence for the important role of chloroplasts in viral RNA synthesis. The chloroplast is considered to be a multifunctional organelle responsible for photosynthesis and for the generation of plant defense signaling molecules. High-throughput technologies (genomics and proteomics), and electron microscopy, including three-dimensional tomography, have revealed that several groups of plant RNA viruses utilize chloroplast membranes to assemble viral replication complexes (VRCs). Moreover, some chloroplast-related proteins reportedly interact with both viral proteins and their genomic RNAs and participate in trafficking these molecules to the chloroplast, where replication occurs. Here, we present the current knowledge on the important role of chloroplasts in the viral replication process.

Keywords: chloroplast; chloroplast membrane; plant-virus interaction; replication; viral replication complex (VRC); viroids.

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Figures

FIGURE 1
FIGURE 1
Schematic illustration of selected host factors affecting viral RNA replication in chloroplasts. Synthesis of viral genomic RNA [(+)ssRNA] requires viral proteins: RdRp (pink circle) and auxiliary factors (green circles) that are translated at the early stage of infection (1). Then, virus recruits host factors (2) such as chaperone (Hsp90), methyltransferase (e.g., PMTS1), chloroplast phosphoglycerate kinase (chlPGK), which participate in viral replication complexes (VRC) targeting (in potexvirus). The 3′UTR of viral RNAs (in potexviruses, e.g., BaMV) interacts with several cellular proteins, including elongation factor 1a (eEF1a), glutathione S-transferase (GSTU4), exonuclease (XRN4). Exonuclease negatively regulates the activity of silencing pathway (miRNA/siRNA). Subsequently, the hijacked host factors, viral genomic RNA and viral proteins are trafficked to chloroplast membranes (3). The ribonucleoprotein complex (RNP) is transported from endoplasmic reticulum (ER) exit sites ERES (in potyvirus) or via targeting proteins, such as Rabs or SNARE (in potexvirus) and actomyosin motility system. Chloroplast membranes are later reorganized to form VRC (4). The panel on the right depicts spherule where the viral RNA is synthesized. The host photosynthetic protein PsbO1 from photosystem II is recruited by potyvirus proteins playing a role in its replication (TVBMV, for details refer to the text). In thylakoid membranes, the β subunit of ATPase has been also involved in VRC assembly (potexvirus and tymovirus). Among viruses, viral RNA of BaMV was observed inside the chloroplast. The presented host factors participate in trafficking to the site of replication or affect (directly or indirectly) the synthesis of viral RNA, that is associated with chloroplast.
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