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      Small RNA-Omics for Plant Virus Identification, Virome Reconstruction, and Antiviral Defense Characterization

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          Abstract

          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 characterization in cultivated and non-cultivated plants. Reviewing available evidence from a large and ever growing number of studies of naturally or experimentally infected hosts revealed that all families of land plant viruses, their satellites and viroids spawn characteristic small RNAs which can be assembled into contigs of sufficient length for virus, satellite or viroid identification and for exhaustive reconstruction of complex viromes. Moreover, the small RNA size, polarity and hotspot profiles reflect virome interactions with the plant RNAi machinery and allow to distinguish between silent endogenous viral elements and their replicating episomal counterparts. Models for the biogenesis and functions of small interfering RNAs derived from all types of RNA and DNA viruses, satellites and viroids as well as endogenous viral elements are presented and discussed.

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          Most cited references174

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          Small silencing RNAs: an expanding universe.

          Since the discovery in 1993 of the first small silencing RNA, a dizzying number of small RNA classes have been identified, including microRNAs (miRNAs), small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). These classes differ in their biogenesis, their modes of target regulation and in the biological pathways they regulate. There is a growing realization that, despite their differences, these distinct small RNA pathways are interconnected, and that small RNA pathways compete and collaborate as they regulate genes and protect the genome from external and internal threats.
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            The expanding world of small RNAs in plants.

            Plant genomes encode various small RNAs that function in distinct, yet overlapping, genetic and epigenetic silencing pathways. However, the abundance and diversity of small-RNA classes varies among plant species, suggesting coevolution between environmental adaptations and gene-silencing mechanisms. Biogenesis of small RNAs in plants is well understood, but we are just beginning to uncover their intricate regulation and activity. Here, we discuss the biogenesis of plant small RNAs, such as microRNAs, secondary siRNAs and heterochromatic siRNAs, and their diverse cellular and developmental functions, including in reproductive transitions, genomic imprinting and paramutation. We also discuss the diversification of small-RNA-directed silencing pathways through the expansion of RNA-dependent RNA polymerases, DICER proteins and ARGONAUTE proteins.
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              Biogenesis, turnover, and mode of action of plant microRNAs.

              MicroRNAs (miRNAs) are small RNAs that control gene expression through silencing of target mRNAs. Mature miRNAs are processed from primary miRNA transcripts by the endonuclease activity of the DICER-LIKE1 (DCL1) protein complex. Mechanisms exist that allow the DCL1 complex to precisely excise the miRNA from its precursor. Our understanding of miRNA biogenesis, particularly its intersection with transcription and other aspects of RNA metabolism such as splicing, is still evolving. Mature miRNAs are incorporated into an ARGONAUTE (AGO) effector complex competent for target gene silencing but are also subjected to turnover through a degradation mechanism that is beginning to be understood. The mechanisms of miRNA target silencing in plants are no longer limited to AGO-catalyzed slicing, and the contribution of translational inhibition is increasingly appreciated. Here, we review the mechanisms underlying the biogenesis, turnover, and activities of plant miRNAs.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                20 November 2018
                2018
                : 9
                : 2779
                Affiliations
                Institut National de la Recherche Agronomique, UMR BGPI , Montpellier, France
                Author notes

                Edited by: Annette Niehl, Julius Kühn-Institut, Germany

                Reviewed by: Carmen Hernandez, Instituto de Biología Molecular y Celular de Plantas (IBMCP), Spain; Francesco Di Serio, Istituto per la Protezione Sostenibile delle Piante, Italy

                *Correspondence: Mikhail M. Pooggin, mikhail.pooggin@ 123456inra.fr

                This article was submitted to Virology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2018.02779
                6256188
                30524398
                ed5d06ac-d135-4e88-80a9-6ec21942711a
                Copyright © 2018 Pooggin.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 October 2018
                : 30 October 2018
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 204, Pages: 20, Words: 0
                Funding
                Funded by: Institut National de la Recherche Agronomique 10.13039/501100006488
                Categories
                Microbiology
                Review

                Microbiology & Virology
                small rna,rna interference,antiviral defense,sirna,next generation sequencing,bioinformatics,virus/viroid diagnostics,virome reconstruction

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