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Ribosome Shunting, Polycistronic Translation, and Evasion of Antiviral Defenses in Plant Pararetroviruses and Beyond Mikhail M

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Ribosome Shunting, Polycistronic Translation, and Evasion of Antiviral Defenses in Plant Pararetroviruses and Beyond Mikhail M Ribosome Shunting, Polycistronic Translation, and Evasion of Antiviral Defenses in Plant Pararetroviruses and Beyond Mikhail M. Pooggin, Lyuba Ryabova To cite this version: Mikhail M. Pooggin, Lyuba Ryabova. Ribosome Shunting, Polycistronic Translation, and Evasion of Antiviral Defenses in Plant Pararetroviruses and Beyond. Frontiers in Microbiology, Frontiers Media, 2018, 9, pp.644. 10.3389/fmicb.2018.00644. hal-02289592 HAL Id: hal-02289592 https://hal.archives-ouvertes.fr/hal-02289592 Submitted on 16 Sep 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - ShareAlike| 4.0 International License fmicb-09-00644 April 9, 2018 Time: 16:25 # 1 REVIEW published: 10 April 2018 doi: 10.3389/fmicb.2018.00644 Ribosome Shunting, Polycistronic Translation, and Evasion of Antiviral Defenses in Plant Pararetroviruses and Beyond Mikhail M. Pooggin1* and Lyubov A. Ryabova2* 1 INRA, UMR Biologie et Génétique des Interactions Plante-Parasite, Montpellier, France, 2 Institut de Biologie Moléculaire des Plantes, Centre National de la Recherche Scientifique, UPR 2357, Université de Strasbourg, Strasbourg, France Viruses have compact genomes and usually translate more than one protein from polycistronic RNAs using leaky scanning, frameshifting, stop codon suppression or reinitiation mechanisms. Viral (pre-)genomic RNAs often contain long 50-leader sequences with short upstream open reading frames (uORFs) and secondary structure elements, which control both translation initiation and replication. In plants, viral RNA and DNA are targeted by RNA interference (RNAi) generating small RNAs that silence viral Edited by: gene expression, while viral proteins are recognized by innate immunity and autophagy Jean-Christophe Paillart, that restrict viral infection. In this review we focus on plant pararetroviruses of the Université de Strasbourg, France family Caulimoviridae and describe the mechanisms of uORF- and secondary structure- Reviewed by: Juan Jose Lopez-Moya, driven ribosome shunting, leaky scanning and reinitiation after translation of short and Consejo Superior de Investigaciones long uORFs. We discuss conservation of these mechanisms in different genera of Científicas (CSIC), Spain Bruno Sargueil, Caulimoviridae, including host genome-integrated endogenous viral elements, as well UMR8015 Laboratoire as in other viral families, and highlight a multipurpose use of the highly-structured leader de Cristallographie et RMN sequence of plant pararetroviruses in regulation of translation, splicing, packaging, and Biologiques, France reverse transcription of pregenomic RNA (pgRNA), and in evasion of RNAi. Furthermore, *Correspondence: Mikhail M. Pooggin we illustrate how targeting of several host factors by a pararetroviral effector protein can [email protected] lead to transactivation of viral polycistronic translation and concomitant suppression of Lyubov A. Ryabova [email protected] antiviral defenses. Thus, activation of the plant protein kinase target of rapamycin (TOR) by the Cauliflower mosaic virus transactivator/viroplasmin (TAV) promotes reinitiation of Specialty section: translation after long ORFs on viral pgRNA and blocks antiviral autophagy and innate This article was submitted to Virology, immunity responses, while interaction of TAV with the plant RNAi machinery interferes a section of the journal with antiviral silencing. Frontiers in Microbiology Keywords: ribosome shunting, leaky scanning, reinitiation, upstream ORF, secondary structure, RNA interference, Received: 24 January 2018 innate immunity, autophagy Accepted: 19 March 2018 Published: 10 April 2018 Citation: INTRODUCTION Pooggin MM and Ryabova LA (2018) Ribosome Shunting, Polycistronic Viruses tend to evolve compact genomes with closely spaced or overlapping protein-coding Translation, and Evasion of Antiviral Defenses in Plant Pararetroviruses sequences and rather short non-coding sequences stuffed with multiple regulatory cis-acting and Beyond. Front. Microbiol. 9:644. elements. This compactness allows for more efficient replication and encapsidation as well as doi: 10.3389/fmicb.2018.00644 successful competition with host mRNAs for translation in the cytoplasm and, in the case of DNA Frontiers in Microbiology | www.frontiersin.org 1 April 2018 | Volume 9 | Article 644 fmicb-09-00644 April 9, 2018 Time: 16:25 # 2 Pooggin and Ryabova Translation and Defense Evasion in Pararetroviruses viruses, with host chromosomes for transcription and replication autophagy, and discuss a possible role of the RTBV protein P4 in in the nucleus. Retroviruses and pararetroviruses that visit suppression of RNAi and innate immunity. both cytoplasm and nucleus during their replication cycles are among the best representatives of such compactness and multipurpose use of regulatory regions of a viral genome THE REGULATORY ROLE OF SHORT 0 (reviewed in Rothnie et al., 1994; Ryabova et al., 2002). Unlike uORFs IN 5 -LEADER REGIONS OF retroviruses, pararetroviruses do not have an obligatory host EUKARYOTIC mRNAs genome integration step, encapsidate into virions a circular dsDNA genome, and replicate via reverse transcription of In eukaryotes, translation is usually initiated via a cap- pgRNA. The pgRNA is transcribed by Pol II from the dependent scanning mechanism (Kozak, 1999, 2002). According circular dsDNA episomes accumulating in the nucleus and then to a current model, the 43S preinitiation scanning complex transported to the cytoplasm for translation and eventually composed of the 40S ribosomal subunit, a ternary complex reverse transcription. (eIF2/GTP/Met-tRNAiMet) and several translation initiation In this review we focus on plant pararetroviruses (family factors (eIF1, eIF1A, eIF3, and eIF5), loaded at the capped 50- Caulimoviridae) that have evolved (i) short upstream (u)ORF- end of mRNA via the multisubunit cap-binding complex eIF4F dependent ribosome shunting to regulate sorting of pregenomic (eIF4E/eIF4G/eIF4A/eIF4B), scans the mRNA leader sequence RNA (pgRNA) for translation and reverse transcription, linearly until the first AUG triplet in a favorable initiation context and (ii) leaky scanning and virus-activated reinitiation to is encountered, where the 60S ribosomal subunit joins to form the make ribosomes translate two and more long ORFs from 80S ribosome and elongation begins (reviewed in Jackson et al., one polycistronic RNA. Using as examples the best studied 2010; Browning and Bailey-Serres, 2015). The favorable initiation pararetroviruses Cauliflower mosaic virus (CaMV; genus context usually contains both R (A or G) at position −3 and Caulimovirus) and Rice tungro bacilliform virus (RTBV; genus G at position C4 with respect of the first nucleotide (nt) of the Tungrovirus), we highlight a multipurpose use of their pgRNA start codon (Kozak, 1986). A substantial fraction of the scanning leader sequence in regulation of ribosome shunting, RNA ribosomes can bypass the first AUG and reach a downstream splicing, packaging and reverse transcription as well as in start codon in a process of leaky scanning if the first AUG evasion of RNAi-based antiviral defense. We also describe an resides in a moderate context missing either R or G at the uORF- and secondary structure-dependent ribosome shunt corresponding positions, or if it is located too close (less than mechanism evolved by other viral families such as animal 10 nts) to the 50-cap (Kozak, 1991). Only a small fraction of (para-)retroviruses (families Hepadnaviridae and Retroviridae) the scanning ribosomes can recognize AUGs residing in a weak and plant RNA picorna-like viruses (family Secoviridae). We then context missing both favorable nts at the positions −3 and C4. describe the mechanisms of polycistronic translation of pgRNA In the cases of weak and moderate contexts of AUG, a secondary in CaMV and RTBV and discuss the conservation of these structure positioned at a short distance of ca. 14 nts downstream mechanisms in different genera of Caulimoviridae, including of the suboptimal start codon can strongly increase efficiency of host genome-integrated endogenous viral elements. Specifically translation initiation, likely by retarding the scanning ribosome we focus on the mechanism of reinitiation after long ORF and thereby providing more time for start codon recognition translation, transactivated by the CaMV TAV protein through its (Kozak, 1990). Notably, translation can be initiated with low interaction with several components of the cellular translation efficiency even at non-AUG start codons which deviate from machinery and activation of the protein kinase TOR. Finally we AUG at one position (e.g., CUG, AUU, etc.) (Gordon et al., describe the mechanisms of CaMV TAV-mediated suppression 1992), and such initiation is facilitated by a favorable initiation of plant antiviral defenses based on RNAi, innate immunity and context, downstream secondary structure, and/or other factors (discussed below). After termination of translation, the 80S Abbreviations: AGO, Argonaute; BFDaV,
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