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Publis18-Bgpi-036 Pooggin Smal Small RNA-Omics for Plant Virus Identification, Virome Reconstruction, and Antiviral Defense Characterization Mikhail Pooggin To cite this version: Mikhail Pooggin. Small RNA-Omics for Plant Virus Identification, Virome Reconstruction, and Antiviral Defense Characterization. Frontiers in Microbiology, Frontiers Media, 2018, 9, 10.3389/fmicb.2018.02779. hal-02624505 HAL Id: hal-02624505 https://hal.inrae.fr/hal-02624505 Submitted on 26 May 2020 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| 4.0 International License fmicb-09-02779 November 16, 2018 Time: 17:10 # 1 REVIEW published: 20 November 2018 doi: 10.3389/fmicb.2018.02779 Small RNA-Omics for Plant Virus Identification, Virome Reconstruction, and Antiviral Defense Characterization Mikhail M. Pooggin* Institut National de la Recherche Agronomique, UMR BGPI, Montpellier, France RNA interference (RNAi)-based antiviral defense generates small interfering RNAs that represent the entire genome sequences of both RNA and DNA viruses as well as viroids and viral satellites. Therefore, deep sequencing and bioinformatics analysis of small RNA population (small RNA-ome) allows not only for universal virus detection and genome reconstruction but also for complete virome reconstruction in mixed infections. Viral infections (like other stress factors) can also perturb the RNAi and gene silencing pathways regulating endogenous gene expression and repressing transposons and host genome-integrated endogenous viral elements which can potentially be released from the genome and contribute to disease. This review describes the application of small RNA-omics for virus detection, virome reconstruction and antiviral defense Edited by: Annette Niehl, characterization in cultivated and non-cultivated plants. Reviewing available evidence Julius Kühn-Institut, Germany from a large and ever growing number of studies of naturally or experimentally infected Reviewed by: hosts revealed that all families of land plant viruses, their satellites and viroids spawn Carmen Hernandez, characteristic small RNAs which can be assembled into contigs of sufficient length Instituto de Biología Molecular y Celular de Plantas (IBMCP), Spain for virus, satellite or viroid identification and for exhaustive reconstruction of complex Francesco Di Serio, viromes. Moreover, the small RNA size, polarity and hotspot profiles reflect virome Istituto per la Protezione Sostenibile delle Piante, Italy interactions with the plant RNAi machinery and allow to distinguish between silent *Correspondence: endogenous viral elements and their replicating episomal counterparts. Models for the Mikhail M. Pooggin biogenesis and functions of small interfering RNAs derived from all types of RNA and [email protected] DNA viruses, satellites and viroids as well as endogenous viral elements are presented Specialty section: and discussed. This article was submitted to Keywords: small RNA, RNA interference, antiviral defense, siRNA, next generation sequencing, bioinformatics, Virology, virus/viroid diagnostics, virome reconstruction a section of the journal Frontiers in Microbiology Received: 01 October 2018 INTRODUCTION Accepted: 30 October 2018 Published: 20 November 2018 Viral small RNAs have been discovered in Nicotiana benthamiana plants inoculated with Citation: potato virus X (genus Potexvirus, family Alphaflexiviridae) using RNA blot hybridization, Pooggin MM (2018) Small and their abundance was found to gradually increase in the time course of viral infection RNA-Omics for Plant Virus (Hamilton and Baulcombe, 1999). A pioneering work of Kreuze et al.(2009) and the follow- Identification, Virome Reconstruction, and Antiviral Defense up studies listed in Supplementary Tables S1, S2 and discussed below have established that Characterization. both RNA and DNA viruses as well as viral satellites and viroids can be identified and Front. Microbiol. 9:2779. their genomes partially or fully reconstructed by deep sequencing and bioinformatic analysis doi: 10.3389/fmicb.2018.02779 of small RNA population (small RNA-ome) from an infected plant. Likewise, small RNA Frontiers in Microbiology| www.frontiersin.org 1 November 2018| Volume 9| Article 2779 fmicb-09-02779 November 16, 2018 Time: 17:10 # 2 Pooggin Small RNA-Omics in Plant Virology deep sequencing can be used for virus detection and assembly plants (compiled in Supplementary Tables S1, S2) revealed of viral genomes from fungi (Vainio et al., 2015; Yaegashi that all 26 families of land plant viruses (Supplementary et al., 2016; Donaire and Ayllón, 2017; Velasco et al., 2018) Table S1 and Supplementary List S1) and 2 families of and from invertebrate animals (Wu et al., 2010; Aguiar et al., viroids (Supplementary Table S2) spawn small RNAs that can 2015; Fung et al., 2018), including insect vectors of the plant be assembled into contigs representing partial or complete viruses transmitted in a propagative manner (Xu et al., 2012; virus/viroid genomes. Such characteristic small RNAs, whose Fletcher et al., 2016; de Haro et al., 2017). Such universality of size-class and polarity profiles (analyzed in many but not the small RNA-omics approach for virus diagnostics is based all cases) are consistent with those of bona fide siRNAs on evolutionary conservation of the small RNA-generating RNA generated by the plant RNAi machinery (described below), interference (RNAi) and gene silencing machinery that regulates have been reported for circular single-stranded (ss)RNA gene expression and defends against invasive nucleic acids viroids replicating in both chloroplasts (Avsunviroidae) and such as transposons, transgenes and viruses in most eukaryotes nuclei (Pospiviroidae) and for viral families with six types of (Ghildiyal and Zamore, 2009; Nayak et al., 2013; tenOever, genomes (Baltimore classification): (i) positive-sense ssRNA 2016). In the case of mammals where an interferon system has [(C)ssRNA: Alphaflexiviridae, Benyviridae, Betaflexiviridae, evolved to limit viral infections, potential contribution of RNAi Bromoviridae, Closteroviridae, Luteoviridae, Potyviridae, to antiviral defenses remains a matter of debates (Jeffrey et al., Secoviridae, Solemoviridae, Tombusviridae, Tymoviridae, 2017; tenOever, 2017). Nonetheless, virus-derived small RNAs Virgaviridae], (ii) negative-sense ssRNA [(−)ssRNA: Aspiviridae, generated by RNAi and/or other mechanisms are detectable Fimoviridae, Phenuiviridae, Rhabdoviridae, Tospoviridae], (iii) by deep sequencing and could be used for virus identification double-stranded RNA [dsRNA: Amalgaviridae, Endornaviridae, in mammals and other vertebrates (Parameswaran et al., 2010; Partitiviridae, Reoviridae], (iv) positive-sense ssRNA replicating Wang F. et al., 2016). via DNA intermediate by reverse transcription [ssRNA-RT: This review article compiles and summarizes growing Metaviridae, Pseudoviridae], (v) single-stranded DNA [ssDNA: evidence demonstrating a universal power of small RNA-omics Geminiviridae, Nanoviridae] and (vi) double-stranded DNA for diagnostics of all types of plant viruses and for exhaustive replicating via RNA intermediate by reverse transcription reconstruction of viromes of various cultivated and non- [dsDNA-RT: Caulimoviridae](Supplementary Tables S1, S2 cultivated plants. Plant virus diagnostics and genome assembly and Supplementary List S1). Likewise, siRNAs have been by high-throughput sequencing of other target nucleic acids such reported for ssRNA satellites (unassigned family) associated as long single-stranded or double-stranded RNA and, in the case with several helper (C)ssRNA viruses from Bromoviridae, of DNA viruses, circular viral DNA enriched by a rolling circle Secoviridae, Tombusviridae, and Virgaviridae as well as for amplification method have been previously reviewed (Boonham ssDNA betasatellites (Tolecusatellitidae) associated with helper et al., 2014; Roossinck et al., 2015; Wu Q. et al., 2015; Jones ssDNA viruses of Geminiviridae (Supplementary Table S1 et al., 2017; Roossinck, 2017; Maliogka et al., 2018; Jeske, 2018). and Supplementary List S1). So far, ssDNA alphasatellites Furthermore, this review illustrates mechanisms of biogenesis (Alphasatellitidae) associated with helper ssDNA viruses of and function of small interfering RNAs (siRNAs) derived from Geminiviridae and Nanoviridae (see Supplementary List S1) plant RNA and DNA viruses, which have been dissected by have not been analyzed by small RNA sequencing. It is deep sequencing and bioinformatics analysis of viral small conceivable that alphasatellites are also targeted by the plant RNA profiles in the model plant Arabidopsis thaliana (family RNAi machinery like their helper viruses. Same assumption Brassicaceae) and its RNAi-deficient mutant lines, and discusses applies to those genera (and species) within the above-listed conservation of these mechanisms in other plant species and plant virus/satellite/viroid families for which small RNA deep families. Finally, the review presents models for biogenesis sequencing data are not available
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