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The 2B Protein of Asparagus Virus 2 Functions As an RNA Silencing Suppressor Against Systemic Silencing to Prove Functional Synteny with Related Cucumoviruses

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The 2B Protein of Asparagus Virus 2 Functions As an RNA Silencing Suppressor Against Systemic Silencing to Prove Functional Synteny with Related Cucumoviruses Virology 442 (2013) 180–188 Contents lists available at SciVerse ScienceDirect Virology journal homepage: www.elsevier.com/locate/yviro The 2b protein of Asparagus virus 2 functions as an RNA silencing suppressor against systemic silencing to prove functional synteny with related cucumoviruses Hanako Shimura n, Chikara Masuta, Naoto Yoshida, Kae Sueda, Masahiko Suzuki Research Faculty of Agriculture, Hokkaido University, Kita 9 Nishi9, Kita-ku, Sapporo 0608589, Japan article info abstract Article history: Asparagus virus 2 (AV-2) is a member of the genus Ilarvirus in the family Bromoviridae. We cloned the coat Received 31 October 2012 protein (CP) and the 2b protein (2b) genes of AV-2 isolates from asparagus plants from various regions Returned to author for revisions and found that the sequence for CP and for 2b was highly conserved among the isolates, suggesting that 5 April 2013 AV-2 from around the world is almost identical. We then made an AV-2 infectious clone by simultaneous Accepted 18 April 2013 inoculation with in vitro transcripts of RNAs 1–3 of AV-2 and in vitro-synthesized CP, which is necessary Available online 13 May 2013 for initial infection. Because 2b of cucumoviruses in Bromoviridae can suppress systemic silencing as well Keywords: as local silencing, we analyzed whether there is functional synteny of 2b between AV-2 and cucumovirus. Asparagus virus 2 Using the AV-2 infectious clone, we here provided first evidence that Ilarvirus 2b functions as an RNA Ilarvirus silencing suppressor; AV-2 2b has suppressor activity against systemic silencing but not local silencing. Genetic variability & 2013 Elsevier Inc. All rights reserved. 2b protein RNA silencing suppressor Introduction prepare AV-2-free asparagus in vitro culture for field production (De Vries-Paterson et al., 1992). To develop a strategy to eliminate Asparagus virus 2 (AV-2) is a member of the genus Ilarvirus and AV-2 from asparagus, we need to elucidate the molecular char- belongs to ilarvirus subgroup 2. Asparagus plants infected with acteristics involved in such mechanisms as seed transmission and AV-2 have no obvious symptoms, but AV-2 infection reduces vigor viral RNA silencing suppression for AV-2. If we can grow AV-2-free and productivity (Elmer et al., 1996; Jaspers et al., 1999; Tomassoli asparagus in fields, we would be able to increase the yield and et al., 2012). AV-2 is transmitted not only through seeds collected quality of asparagus. Toward this endeavor, we here investigated from infected asparagus, but also through seeds collected from whether AV-2 was still present in asparagus fields in Japan and healthy plants fertilized by AV-2-infected pollens; AV-2 is not then initiated the molecular study of AV-2. transmitted by aphids (Elmer et al., 1996; Jaspers and Pearson, The genus Ilarvirus is included in the family Bromoviride,which 1997). In addition, AV-2 is mechanically transmitted mainly also includes cucumoviruses and bromoviruses, some of the most through infected sap on cutting knives and probably through extensively studied plant viruses. All members have a tripartite RNA feeding thrips as shown for other ilarviruses (Greber et al., 1991). genome (RNAs 1–3). RNA 1 encodes the 1a protein with methyl- AV-2 infection of asparagus has been reported in Europe, North transferase and helicase motifs. RNA 2 encodes the 2a protein, America and Japan (Elmer et al., 1996; Uyeda and Mink, 1981). which is an RNA-dependent-RNA polymerase (RdRp). RNA 2 of Fujisawa et al. (1983) first identified AV-2 in the asparagus fields of some members (i.e., cucumoviruses and subgroup 1 and 2 in Hokkaido, the largest production area in Japan, and named the ilarviruses) has a second gene encoding the 2b protein (2b) (Xin Japanese isolate AV-2-J. In spite of the serious distribution, AV-2 et al., 1998), which is expressed through a subgenomic RNA, RNA4A. infection has not been surveyed for the last few decades in Neither alfamoviruses nor bromoviruses in the Bromoviride have Hokkaido as well as in other areas in Japan. In addition, the been found to encode the 2b protein. In cucumoviruses, 2b has been production of virus-free asparagus has not been attempted until shown to be an RNA silencing suppressor (RSS) (Burgyán and now because AV-2 infection reduces the rooting and survival of Havelda, 2011), but whether the 2b of ilarvirus functions as an asparagus explants in vitro, suggesting that it is not easy to RSS has not been known. RNA 3 encodes the movement protein (MP) in the 5′ half and the coat protein (CP) in the 3′ half. The CP, expressed by subgenomic RNA4, is necessary for genome activation n Corresponding author. Fax: +81 11 706 3634. for alfamovirus and ilarviruses (Jaspars, 1999; Neeleman et al., E-mail address: [email protected] (H. Shimura). 2004), suggesting the possibility that replication of ilarviruses is 0042-6822/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.virol.2013.04.015 H. Shimura et al. / Virology 442 (2013) 180–188 181 Tobacco mosaic virus (TMV) NP_597750 Tomato mosaic virus (ToMV) CAA26084 Olive latent virus 1 (OLV-1) AAU09671 Oleavirus Cucumber mosaic virus (CMV) CAH17692 100 Peanut stunt virus (PSV) CAX30778 Cucumovirus 99 Tomato aspermy virus (TAV) ABM73664 Pelargonium zonate spot virus (PZSV) ACG63773 Anulavirus Brome mosaic virus (BMV) AAA46334 100 Bromovirus 100 Spring beauty latent virus (SMLV) BAC10648 Prune dwarf virus (PDV) ABQ95996 Ilarvirus (4) Apple mosaic virus (ApMV) AAT11877 Ilarvirus (3) Prunus necrotic ringspot virus (PNRSV) AAA96660 American plum line pattern virus (APLPV) AAK15030 Ilarvirus (5) 100 Fragaria chiloensis latent virus (FCILV) YP_164805 Ilarvirus (6) Humulus japonicus latent virus (HJLV) AAS86441 Ilarvirus (3) Alfalfa mosaic virus (AMV) AAG10218 Alfamovirus Parietaria mottle virus (PMoV) CAJ58674 100 Tomato necrotic spot virus ACI96015 Ilarvirus (1) 100 100 Tobacco streak virus (TSV) ACJ38091 Strawberry necrotic shock virus (SNSV) AAQ76587 76 Blackberry chlorotic ringspot virus (BCRV) AAZ42394 100 Lilac ring mottle virus (LRMV) AAA64840 Citrus leaf rugose virus (CiLRV) NP_613280 Tulare apple mosaic virus (TAMV) NP_620757 87 Spinach latent virus (SpLV) NP_620681 100 Elm mottle virus (EMoV) AAB97771 Hydrangea mosaic virus (HdMV) AAF89808 74 Citrus variegation virus (CVV) ACC62166 Citrus variegation virus (CVV) AAL37959 Ilarvirus (2) AV-2 JP-Iw AB745625 90 AV-2 JP-Ha AB745623 0.1 AV-2 Peru AB745626 AV-2 JP-Ku AB745624 100 AV-2 Australia AB745627 AV-2 Mexico2 AB745629 AV-2 Mexico1 AB745628 Asparagus virus 2 (AV2) YP_002455927 Fig. 1. Phylogenetic relationships among the nucleotide sequences of the CP genes from representative ilarviruses and related viruses in the Bromoviridae. The trees were constructed by the maximum-likelihood method implemented in the PAUP 4.0 software. Bootstrap values (1000 replicates) are given at branch points (only values 470 are shown). The evolutionary-distance scale is the number of substitutions per site. Tobacco mosaic virus (TMV) and Tomato mosaic virus (ToMV) were used as outgroups. AV-2 isolates from Japan (JP-Ku, JP-Ha and JP-Iw), Australia, Mexico and Peru in bold face were newly sequenced in this study. closely related to that of alfamoviruses. In fact, functional similarity developed an efficient method to synthesize infectious transcripts via of CPs of Alfalfa mosaic virus (AMV, alfamovirus) and Tobacco streak genome activation by in vitro-synthesized CP, and we also found that virus (TSV, ilarvirus) has been demonstrated; the two viral CPs share AV-2 2b functioned as a systemic RSS. This is the first demonstration a limited, unique consensus sequence (Ansel-McKinney et al., 1996; that Ilarvirus 2b functions as an RSS similar to the 2b of cucumoviruses Swanson et al., 1998). in Bromoviridae. We discuss the implications of AV-2 2b as an RSS Cucumber mosaic virus (CMV) isolates, which belong to against systemic silencing and contributions to unique AV-2 charac- Bromoviridae, are divided into two subgroups I and II based on the teristics such as latent infection and seed transmission. nucleotide and amino acid sequence of the viral genes. The 2b genes in subgroups I and II functionally differ in silencing suppressor activity; 2b of subgroup I has a stronger RSS activity than that of Results subgroup II. Because among the viruses in Bromoviridae,only cucumoviruses and ilarviruses have a 2b gene, the function of 2b Genetic variability of AV-2 isolates of AV-2 is of our particular interest: there is the possibility that AV-2 isolates might be also divided into some subgroups just like CMV, In preliminary RT-PCR experiments, we detected AV-2 from the and AV-2 2b thus shows functional synteny to the 2b of cucumo- commercial asparagus from different asparagus-growing areas in viruses. For AV-2 isolates, two serotypes (AV-2-P and AV-2-S) that Japan and other countries. For our phylogenetic analysis, we here vary in their infectivity on Chenopodium quinoa have been reported cloned the CP (654 nt) and 2b (582 nt) genes from infected for AV-2 (Uyeda and Mink, 1981), suggesting that variability in the asparagus spears obtained from different geographic locations: nucleotide sequences for the viral genes could explain serological Japanese asparaguses (from Kuriyama [Hokkaido], Hakodate and symptomatic differences. Because only one sequence for the CP [Hokkaido] and Iwate [Honshu]) and imported asparagus (from and the 2b genes of AV-2 are available in the database, there is no Peru, Mexico and Australia). The CP and the 2b genes from each molecular evidence for the genetic variability of AV-2 (Rafael-Martín isolate (at least 5 clones) were sequenced to avoid nucleotide and Rivera-Bustamante, 1999; Scott and Zimmerman, 2009; changes due to PCR errors. Multiple alignments of the CP and 2b Tomassoli et al., 2012).
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