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Variability Studies of Two Prunus-Infecting Fabaviruses with the Aid of High-Throughput Sequencing

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Variability Studies of Two Prunus-Infecting Fabaviruses with the Aid of High-Throughput Sequencing Variability Studies of Two Prunus-Infecting Fabaviruses with the Aid of High-Throughput Sequencing. Igor Koloniuk, Tatiana Sarkisova, Karel Petrzik, Ondřej Lenz, Jaroslava Přibylová, Jana Fránová, Leonidas Lotos, Christina Beta, Asimina Katsiani, Thierry Candresse, et al. To cite this version: Igor Koloniuk, Tatiana Sarkisova, Karel Petrzik, Ondřej Lenz, Jaroslava Přibylová, et al.. Variability Studies of Two Prunus-Infecting Fabaviruses with the Aid of High-Throughput Sequencing.. Viruses, MDPI, 2018, 10 (4), pp.204. 10.3390/v10040204. hal-02624929 HAL Id: hal-02624929 https://hal.inrae.fr/hal-02624929 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 viruses Article Variability Studies of Two Prunus-Infecting Fabaviruses with the Aid of High-Throughput Sequencing Igor Koloniuk 1,* ID , Tatiana Sarkisova 1, Karel Petrzik 1 ID , OndˇrejLenz 1, Jaroslava Pˇribylová 1, Jana Fránová 1 ID , Josef Špak 1, Leonidas Lotos 2, Christina Beta 2, Asimina Katsiani 2, Thierry Candresse 3 and Varvara I. Maliogka 2 ID 1 Department of Plant Virology, Institute of Plant Molecular Biology, Biology Centre of the Academy of Sciences of the Czech Republic, v.v.i., 370 05 Ceskˇ é Budˇejovice,Czech Republic; [email protected] (T.S.); [email protected] (K.P.); [email protected] (O.L.); [email protected] (J.P.); [email protected] (J.F.); [email protected] (J.Š.) 2 Laboratory of Plant Pathology, School of Agriculture, Faculty of Agriculture, Forestry and Natural Environment, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece; [email protected] (L.L.); [email protected] (C.B.); [email protected] (A.K.); [email protected] (V.I.M.) 3 UMR 1332 Biologie du Fruit et Pathologie, INRA, University of Bordeaux, CS20032, F-33882 Villenave d’Ornon CEDEX, France; [email protected] * Correspondence: [email protected]; Tel.: +420-387-775-531 Received: 22 March 2018; Accepted: 14 April 2018; Published: 18 April 2018 Abstract: During their lifetime, perennial woody plants are expected to face multiple infection events. Furthermore, multiple genotypes of individual virus species may co-infect the same host. This may eventually lead to a situation where plants harbor complex communities of viral species/strains. Using high-throughput sequencing, we describe co-infection of sweet and sour cherry trees with diverse genomic variants of two closely related viruses, namely prunus virus F (PrVF) and cherry virus F (CVF). Both viruses are most homologous to members of the Fabavirus genus (Secoviridae family). The comparison of CVF and PrVF RNA2 genomic sequences suggests that the two viruses may significantly differ in their expression strategy. Indeed, similar to comoviruses, the smaller genomic segment of PrVF, RNA2, may be translated in two collinear proteins while CVF likely expresses only the shorter of these two proteins. Linked with the observation that identity levels between the coat proteins of these two viruses are significantly below the family species demarcation cut-off, these findings support the idea that CVF and PrVF represent two separate Fabavirus species. Keywords: plant virus; fabavirus; novel species; prunus; high-throughput sequencing; intrahost variability; phylogenetics 1. Introduction Fruit trees are known to be hosts to a high number of viruses, mainly as a result of their vegetative mode of propagation and long-term cultivation in orchards. Especially in Prunus, several new viral species were described in recent years with the aid of high-throughput sequencing (HTS) [1,2]. In 2011, 23 different viruses were known to infect sweet and sour cherry worldwide [3]. This number is constantly increasing and includes viruses belonging to genera that were previously unknown to infect Prunus species [4,5]. It was pointed out that mixed infections of Prunus sp., and cherry species in particular, are frequent and thus hamper the determination of pathogen-symptoms correlation [1]. Moreover, it was shown that in several occasions the intra-host population of a Prunus infecting virus Viruses 2018, 10, 204; doi:10.3390/v10040204 www.mdpi.com/journal/viruses Viruses 2018, 10, 204 2 of 13 species might be highly heterogeneous, consisting of distant genetic variants [6] with yet unknown implications on the virus pathogenicity and epidemiology. Existing HTS methodologies already have satisfactory sequencing capacity for the study of such heterogeneous viral populations. For instance, when artificial mixtures of five human immunodeficiency virus 1 genotypes were subjected to HTS, comparable results were produced with different sequencing platforms (Roche 454pyrosequencing, Solexa by Illumina, Single-molecule real-time sequencing by PacBio). In such a situation, the existence of low complexity regions may represent an obvious obstruction for the assembly step of genetically close genotypes [7]. In the present study, we molecularly characterized two closely related viruses of the genus Fabavirus, family Secoviridae, which were found by HTS to infect cherry trees as mixtures of genotypes. Fabaviruses are single-stranded positive sense RNA viruses with two genomic segments (RNA1 and RNA2). Each RNA encodes a polyprotein which is proteolytically cleaved into the functional proteins. RNA1 contains the nucleoside triphosphate (NTP)-binding, genome-linked protein (VPg), proteinase and polymerase motifs, whereas RNA2 has the movement (MP) and capsid (CP) proteins motifs [8]. During their replication, large protein complexes, associated with endoplasmic reticulum-derived membranes, are formed in infected cells. Fabaviruses have a wide host range among some monocotyledonous and many dicotyledonous families and they are known to be aphid-transmitted in the non-persistent manner [8]. Nevertheless, the genus is not numerous: there are only seven recognized virus species to date. The first fabavirus characterized in sweet cherries and studied herein, prunus virus F (PrVF), was described by Villamor et al. [4] and has recently been reported in the Czech Republic [9]. The second one is presumably a novel virus species, genetically close to PrVF, which was tentatively named cherry virus F (CVF) and is reported here for the first time. CVF was detected in plant materials from the Czech Republic and Greece. The phylogenetic relationships between these two viruses are analyzed and the factors that are putatively shaping their evolution and their frequent existence as mixtures of different variants are discussed. 2. Materials and Methods The majority of samples from cherry trees were collected during 2014–2016 from four locations. Six samples were taken from the germplasm at the Research and Breeding Institute of Pomology, Holovousy, Czech Republic (50.3683644N, 15.5675814E). Two samples, SwC–H and SwC–H6, were collected in South Bohemia region (49.1512472N, 14.4814483E and 49.049139N, 14.4589956E, respectively), approximately 10 km each from the other and 160 km away from the Holovousy village. One sample was collected in 2009, from a sweet cherry orchard in Aridaia, Pella in Greece (Table1). Selected specimens were subjected to (a) enrichment of double-stranded RNA (dsRNA) species as described previously [10], (b) isolation of either total RNA and subsequent messenger RNA (polyA) enrichment (MagJET Plant RNA Purification Kit, MagJET mRNA Enrichment Kit, Thermo Scientific, Vilnius, Lithuania) or (c) isolation of small RNAs using mirPremier microRNA Isolation Kit (Sigma-Aldrich, St. Louis, MO, USA) (Table1). Enriched dsRNA was extracted following cellulose-based protocol with slight modifications, which included optional S1 nuclease (Thermo Scientific) and TURBO DNase (Life Technologies, Carlsbad, CA, USA) treatments. Quantification and quality controls were done with Nanodrop spectrophotometer and/or Qubit fluorometr and native agarose electrophoresis, respectively. Library preparations were done either externally with TrueSeq Illumina kit or internally with MuSeek Library preparation kit (Thermo Scientific) and subjected to HiSeq2500 sequencing (service provider SeqMe s.r.o., Dobˇríš, Czech Republic). Small RNAs library construction and sequencing were performed by Life Sequencing S.L. (Paterna, Spain) on an Ion Torrent platform using the Ion 318TM chip (South San Francisco, CA, USA). The obtained sequence reads were quality trimmed and de novo assembled using CLC Genomic Workbench 8.5.1 (Qiagen, Sverige, Denmark). Verification of assembly consistency was done by back-mapping of trimmed reads onto reference sequences with following parameters—coverage Viruses 2018, 10, 204 3 of 13 fraction minimum 0.5, identity 0.95. Continuity of the assemblies was visually verified for covering inconsistencies. Total RNA was extracted from 50 mg of fresh leaf material using a MagJET Plant RNA Kit (Thermo Scientific) and transcribed into complementary DNA (cDNA) with random hexamers and Maxima H Minus First Strand cDNA Synthesis Kit (Thermo Scientific) according to the manufacturer’s recommendations.
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