Virus diseases of strawberry present several complex problems. More than 25 viruses have been described in the genus Fragaria thus far. Here, we describe a novel rhabdovirus, tentatively named strawberry virus 1 (StrV-1), that infects F.ananassa and F.vesca plants. Genomic sequences of three distinct StrV-1 genotypes co-infecting a single F.ananassa host were obtained using combined Illumina and Ion Proton high-throughput sequencing. StrV-1 was transmitted to herbaceous plants via Aphisfabae and A.ruborum, further mechanically transmitted to Nicotianaoccidentalis 37B and sub-inoculated to N.benthamiana, N.benthamiana DCL2/4i, N.occidentalis 37B, and Physalisfloridana plants. Irregular chlorotic sectors on leaf blades and the multiplication of calyx leaves seem to be the diagnostic symptoms for StrV-1 on indexed F.vesca clones. StrV-1 was detected in asymptomatic grafted plants and in 49 out of 159 field strawberry samples via RT-PCR followed by Sanger sequencing. The bacilliform shape of the virions, which have a cytoplasm-limited distribution, their size, and phylogenetic relationships support the assignment of StrV-1 to a distinct species of the genus Cytorhabdovirus. Acyrthosiphonmalvae, A.fabae, and A.ruborum were shown to transmit StrV-1 under experimental conditions.

Department of Plant Virology Institute of Plant Molecular Biology Biology Centre Czech Academy of Sciences 370 05 České Budějovice Czech Republic

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Hancock J.F. Temperate Fruit Crops in Warm Climates. Volume 69. Springer Netherlands; Dordrecht, The Netherlands: 2000. Strawberries; pp. 445–455.

Martin R.R., Tzanetakis I.E. Characterization and Recent Advances in Detection of Strawberry Viruses. Plant Dis. 2006;90:384–396. doi: 10.1094/PD-90-0384. PubMed DOI

Converse R.H. In: Virus Disease of Small Fruits. Converse R.H., editor. United States Department of Agriculture; Washington, DC, USA: 1987. pp. 1–288.

Conci V.C., Luciani C.E., Merino M.C., Celli M.G., Perotto M.C., Torrico A.K., Pozzi E., Strumia G., Dughetti A.C., Asinari F., et al. Advances in characterization and epidemiology of strawberry viruses and phytoplasmas in Argentina. Acta Hortic. 2017:801–810. doi: 10.17660/ActaHortic.2017.1156.118. DOI

Barritt B.H., Loo H.Y.S. Effects of mottle, crinkle, and mild yellow-edge viruses on growth and yield of hood and northwest strawberries. Can. J. Plant Sci. 1973;53:605–607. doi: 10.4141/cjps73-119. DOI

Bolton A.T. Effects of three virus diseases and their combinations on fruit yield of strawberries. Can. J. Plant Sci. 1974;54:271–275. doi: 10.4141/cjps74-043. DOI

Babovic M.V. Changes in the yield and quality of strawberry fruits infected by strawberry crinkle virus. Acta Hortic. 1976:25–28. doi: 10.17660/ActaHortic.1976.66.2. DOI

Aerts J. Effect of strawberry mild yellow-edge virus on the production of strawberries. Mededelingen Faculteit Landbouwwetenschappen Gent. 1980;45:369–375.

Maas J.L. Compendium of strawberry diseases. 2nd ed. APS Press; St. Paul, MN, USA: 1998.

Martin R.R., Tzanetakis I.E. High risk strawberry viruses by region in the United States and Canada: Implications for certification, nurseries, and fruit production. Plant Dis. 2013;97:1358–1362. doi: 10.1094/PDIS-09-12-0842-RE. PubMed DOI

Xiang Y., Bernardy M., Bhagwat B., Wiersma P.A., DeYoung R., Bouthillier M. The complete genome sequence of a new polerovirus in strawberry plants from eastern Canada showing strawberry decline symptoms. Arch. Virol. 2015;160:553–556. doi: 10.1007/s00705-014-2267-0. PubMed DOI

Torrico A.K., Salazar S.M., Kirschbaum D.S., Conci V.C. Yield losses of asymptomatic strawberry plants infected with Strawberry mild yellow edge virus. Eur. J. Plant Pathol. 2017;150:983–990. doi: 10.1007/s10658-017-1337-z. DOI

Ma X., Cui H., Bernardy M., Tian L., Abbasi P., Wang A. Molecular characterization of a Strawberry mild yellow edge virus isolate from Canada. Can. J. Plant Pathol. 2015;37:369–375. doi: 10.1080/07060661.2015.1053990. DOI

Tzanetakis I.E., Martin R.R. Strawberry chlorotic fleck: Identification and characterization of a novel Closterovirus associated with the disease. Virus Res. 2007;124:88–94. doi: 10.1016/j.virusres.2006.10.005. PubMed DOI

Chen L., Shang Q.X., Chen X.Y., Xing D.M., Yang R., Han C.G., Ran C., Wei Y.M., Zhao X.Y., Liu Z.P. First report on the occurrence of cucumber mosaic virus on Fragaria ananassa in China. Plant Dis. 2014;98:1015. doi: 10.1094/PDIS-11-13-1173-PDN. PubMed DOI

Thekke-Veetil T., Tzanetakis I.E. First Report of Strawberry polerovirus-1 in Strawberry in the United States. Plant Dis. 2016;100:867. doi: 10.1094/PDIS-09-15-1044-PDN. DOI

Luciani C.E., Celli M.G., Merino M.C., Perotto M.C., Pozzi E., Conci V.C. First Report of Strawberry polerovirus 1 in Argentina. Plant Dis. 2016;100:1510. doi: 10.1094/PDIS-10-15-1213-PDN. DOI

Ding X., Li Y., Hernández-Sebastià C., Abbasi P.A., Fisher P., Celetti M.J., Wang A. First Report of Strawberry crinivirus 4 on Strawberry in Canada. Plant Dis. 2016;100:1254. doi: 10.1094/PDIS-01-16-0009-PDN. DOI

Chen D., Ding X., Wang A., Zhang J., Wu Z. First report of strawberry crinivirus 3 and strawberry crinivirus 4 on strawberry in China. New Dis. Rep. 2018;37:24. doi: 10.5197/j.2044-0588.2018.037.024. DOI

Walker P.J., Blasdell K.R., Calisher C.H., Dietzgen R.G., Kondo H., Kurath G., Longdon B., Stone D.M., Tesh R.B., Tordo N., et al. ICTV Virus Taxonomy Profile: Rhabdoviridae. J. Gen. Virol. 2018;99:447–448. doi: 10.1099/jgv.0.001020. PubMed DOI

Jackson A.O., Dietzgen R.G., Goodin M.M., Bragg J.N., Deng M. Biology of plant rhabdoviruses. Annu. Rev. Phytopathol. 2005;43:623–660. doi: 10.1146/annurev.phyto.43.011205.141136. PubMed DOI

Ammar E.-D., Tsai C.-W., Whitfield A.E., Redinbaugh M.G., Hogenhout S.A. Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Ann. Rev. Entomol. 2009;54:447–468. doi: 10.1146/annurev.ento.54.110807.090454. PubMed DOI

Todd J.C., Ammar E.-D., Redinbaugh M.G., Hoy C., Hogenhout S.A. Plant host range and leafhopper transmission of Maize fine streak virus. Phytopathology. 2010;100:1138–1145. doi: 10.1094/PHYTO-05-10-0144. PubMed DOI

Kormelink R., Garcia M.L., Goodin M., Sasaya T., Haenni A.-L. Negative-strand RNA viruses: The plant-infecting counterparts. Virus Res. 2011;162:184–202. doi: 10.1016/j.virusres.2011.09.028. PubMed DOI

Walker P.J., Dietzgen R.G., Joubert D.A., Blasdell K.R. Rhabdovirus accessory genes. Virus Res. 2011;162:110–125. doi: 10.1016/j.virusres.2011.09.004. PubMed DOI PMC

Dietzgen R.G., Kondo H., Goodin M.M., Kurath G., Vasilakis N. The family Rhabdoviridae: Mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins. Virus Res. 2017;227:158–170. doi: 10.1016/j.virusres.2016.10.010. PubMed DOI PMC

Yoshikawa N., Inouye T., Converse R.H. Two types of rhabdovirus in strawberry. Jpn. J. Phytopathol. 1986;52:437–444. doi: 10.3186/jjphytopath.52.437. DOI

Koloniuk I., Fránová J., Sarkisova T., Přibylová J. Complete genome sequences of two divergent isolates of strawberry crinkle virus coinfecting a single strawberry plant. Arch Virol. 2018;163:2539–2542. doi: 10.1007/s00705-018-3860-4. PubMed DOI

Yao H., Song J., Liu C., Luo K., Han J., Li Y., Pang X., Xu H., Zhu Y., Xiao P., et al. Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS ONE. 2010;5:e13102. doi: 10.1371/journal.pone.0013102. PubMed DOI PMC

Harry M., Solignac M., Lachaise D. Molecular evidence for parallel evolution of adaptive syndromes in fig-breeding Lissocephala (Drosophilidae) Mol. Phylogenetics Evol. 1998;9:542–551. doi: 10.1006/mpev.1998.0508. PubMed DOI

Thompson J.R., Wetzel S., Klerks M.M., Vašková D., Schoen C.D., Špak J., Jelkmann W. Multiplex RT-PCR detection of four aphid-borne strawberry viruses in Fragaria spp. in combination with a plant mRNA specific internal control. J. Virol. Methods. 2003;111:85–93. doi: 10.1016/S0166-0934(03)00164-2. PubMed DOI

Koloniuk I., Fránová J., Sarkisova T., Přibylová J., Lenz O., Petrzik K., Špak J. Identification and molecular characterization of a novel varicosa-like virus from red clover. Arch. Virol. 2018;163:2213–2218. doi: 10.1007/s00705-018-3838-2. PubMed DOI

Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T.L. BLAST+: Architecture and applications. BMC Bioinform. 2009;10:421. doi: 10.1186/1471-2105-10-421. PubMed DOI PMC

Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., et al. Phylogeny.fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36:W465–W469. doi: 10.1093/nar/gkn180. PubMed DOI PMC

Letunic I., Bork P. Interactive tree of life (iTOL) v3: An online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44:W242–W245. doi: 10.1093/nar/gkw290. PubMed DOI PMC

Marchler-Bauer A., Bo Y., Han L., He J., Lanczycki C.J., Lu S., Chitsaz F., Derbyshire M.K., Geer R.C., Gonzales N.R., et al. CDD/SPARCLE: Functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–D203. doi: 10.1093/nar/gkw1129. PubMed DOI PMC

Krogh A., Larsson B., von Heijne G., Sonnhammer E.L.L. Predicting transmembrane protein topology with a hidden markov model: Application to complete genomes. J. Mol. Biol. 2001;305:567–580. doi: 10.1006/jmbi.2000.4315. PubMed DOI

Dadami E., Boutla A., Vrettos N., Tzortzakaki S., Karakasilioti I., Kalantidis K. DICER-LIKE 4 but not DICER-LIKE 2 may have a positive effect on potato spindle tuber viroid accumulation in Nicotiana benthamiana. Mol. Plant. 2013;6:232–234. doi: 10.1093/mp/sss118. PubMed DOI

Frazier N.W. Detection of graft-transmissible diseases in strawberry by a modified leaf grafting technique. Plant Dis. Report. 1974;58:203–207.

Fránova Honetšlegrová J., Vibio M., Bertaccini A. Electron microscopy and molecular identification of phytoplasmas associated with strawberry green petals in the Czech Republic. Eur. J. Plant Pathol. 1996;102:831–835. doi: 10.1007/BF01877052. DOI

Fránová J., Sarkisová T., Jakešová H., Koloniuk I. Molecular and biological properties of two putative new cytorhabdoviruses infecting Trifolium pratense. Plant Pathol. 2019;11:90–1286. doi: 10.1111/ppa.13065. DOI

International Committee on Taxonomy of Viruses (ICTV) [(accessed on 1 October 2019)]; Available online: https://talk.ictvonline.org/files/proposals/taxonomy_proposals_plant1/m/plant04/9195.

Thompson J.R., Jelkmann W. The detection and variation of Strawberry mottle virus. Plant Dis. 2003;87:385–390. doi: 10.1094/PDIS.2003.87.4.385. PubMed DOI

Ding X., Chen D., Du Z., Zhang J., Wu Z. The complete genome sequence of a novel cytorhabdovirus identified in strawberry (Fragaria ananassa Duch.) Arch Virol. 2019:1–5. doi: 10.1007/s00705-019-04390-y. PubMed DOI

Richardson J., Frazier N.W., Sylvester E.S. Rhabdoviruslike particles associated with strawberry crinkle virus. Phytopathology. 1972;62:491–492. doi: 10.1094/Phyto-62-491. DOI

Hunter B.G., Richardson J., Dietzgen R.G., Karu A., Sylvester E.S., Jackson A.O., Morris T.J. Purification and Characterization of Strawberry Crinkle Virus. Phytopathology. 1990;80:282–287. doi: 10.1094/Phyto-80-282. DOI

Fránová-Honetšlegrová J., Erbenová M. The discovery of rhabdovirus-like particles in strawberry in the Czech Republic. Acta Virol. 1999;43:271–272. PubMed

Matthews R.E.F. In: Plant Virology. 3rd ed. Matthews R.E.F., editor. Academic Press; San Diego, CA, USA: 1991.

Plantwise Knowledge Bank—Chaetosiphon fragaefolii. [(accessed on 10 July 2019)]; Available online: https://www.plantwise.org/knowledgebank/datasheet/13305#DistributionSection.

Holman J. Host Plant Catalog of Aphids. Springer; Dordrecht, The Netherlands: 2009.

Analysis of Virus-Derived siRNAs in Strawberry Plants Co-Infected with Multiple Viruses and Their Genotypes

Transmission of Diverse Variants of Strawberry Viruses Is Governed by a Vector Species

Identification and Characterization of a Novel Umbra-like Virus, Strawberry Virus A, Infecting Strawberry Plants

High Incidence of Strawberry Polerovirus 1 in the Czech Republic and Its Vectors, Genetic Variability and Recombination

2021 Taxonomic update of phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales