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Review
. 2017 Dec 11:8:2093.
doi: 10.3389/fpls.2017.02093. eCollection 2017.

Plant RNA Regulatory Network and RNA Granules in Virus Infection

Affiliations
Review

Plant RNA Regulatory Network and RNA Granules in Virus Infection

Kristiina Mäkinen et al. Front Plant Sci. .

Abstract

Regulation of post-transcriptional gene expression on mRNA level in eukaryotic cells includes translocation, translation, translational repression, storage, mRNA decay, RNA silencing, and nonsense-mediated decay. These processes are associated with various RNA-binding proteins and cytoplasmic ribonucleoprotein complexes many of which are conserved across eukaryotes. Microscopically visible aggregations formed by ribonucleoprotein complexes are termed RNA granules. Stress granules where the translationally inactive mRNAs are stored and processing bodies where mRNA decay may occur present the most studied RNA granule types. Diverse RNP-granules are increasingly being assigned important roles in viral infections. Although the majority of the molecular level studies on the role of RNA granules in viral translation and replication have been conducted in mammalian systems, some studies link also plant virus infection to RNA granules. An increasing body of evidence indicates that plant viruses require components of stress granules and processing bodies for their replication and translation, but how extensively the cellular mRNA regulatory network is utilized by plant viruses has remained largely enigmatic. Antiviral RNA silencing, which is an important regulator of viral RNA stability and expression in plants, is commonly counteracted by viral suppressors of RNA silencing. Some of the RNA silencing suppressors localize to cellular RNA granules and have been proposed to carry out their suppression functions there. Moreover, plant nucleotide-binding leucine-rich repeat protein-mediated virus resistance has been linked to enhanced processing body formation and translational repression of viral RNA. Many interesting questions relate to how the pathways of antiviral RNA silencing leading to viral RNA degradation and/or repression of translation, suppression of RNA silencing and viral RNA translation converge in plants and how different RNA granules and their individual components contribute to these processes. In this review we discuss the roles of cellular RNA regulatory mechanisms and RNA granules in plant virus infection in the light of current knowledge and compare the findings to those made in animal virus studies.

Keywords: RNA Interference; mRNA decay; nonsense mediated mRNA decay; plant viruses; processing bodies; siRNA bodies; stress granules.

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Figures

Figure 1
Figure 1
Major RNA regulatory processes in plant cells. Host mRNAs carrying the 5′ cap and the 3′ poly(A) tail are recruited to ribosomes for translation. vRNAs have evolved means to regulate host translation for their benefit. Various cellular stresses create SGs and increase the size and number of PBs. Translationally stalled pre-initiation complexes condense into SGs and can be released back to translation when stress conditions disappear. RNAs lacking the 5′ cap and the 3′ poly(A) tail are targeted for decay whereas translationally repressed RNAs can be redirected from PBs back to translation. PBs and SGs dock, fuse and exchange material. vRNAs and mRNAs recognized by the RNA silencing and NMD machineries are targeted for degradation. The RNA silencing functions are partially located to siRNA bodies and NMD to PBs. siRNA bodies can associate with PBs and SGs during stress. Only the main components of each granule type are shown. PB, processing body; SG, stress granule; NMD, nonsense-mediated decay; PTC, premature termination codon; VRC, virus replication complex.
Figure 2
Figure 2
Plant virus interactions with RNP granules. (A) Cabbage leaf curl virus nuclear-cytosol shuttle protein BV1 can bind to the promoter region of AS2 gene and induce its expression. AS2 is transported with BV1 to PBs where it activates DCP2-mediated decapping. Increased RNA decay down-regulates RNA silencing and consequently virus infection gets advantage. (B) Potato virus A silencing suppressor protein HCPro induces formation of RNP granules that contain viral RNA, ribosomal protein P0 and several PB and SG markers. Viral protein genome-linked, VPg, abolishes PVA-induced granules and increases viral translation. Evidence to support silencing suppression-related PG functions exists. (C) Brome mosaic virus genomic RNAs 2 and 3 contain motifs for binding to the decapping activator LSm1-7 complex in PBs of yeast. This interaction is required both for brome mosaic virus translation and replication. In the absence of viral protein 1a vRNA is subjected to translation whereas in its presence vRNA is recruited to replication.

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