Transmission of Diverse Variants of Strawberry Viruses Is Governed by a Vector Species
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35891344
PubMed Central
PMC9316375
DOI
10.3390/v14071362
PII: v14071362
Knihovny.cz E-zdroje
- Klíčová slova
- aphid transmission, multiple infections, plant virus, strawberry virus,
- MeSH
- jahodník * MeSH
- mšice * MeSH
- nemoci rostlin MeSH
- Rhabdoviridae * genetika MeSH
- Secoviridae * MeSH
- virové nemoci * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Advances in high-throughput sequencing methods have boosted the discovery of multistrain viral infections in diverse plant systems. This phenomenon appears to be pervasive for certain viral species. However, our knowledge of the transmission aspects leading to the establishment of such mixed infections is limited. Recently, we reported a mixed infection of a single strawberry plant with strawberry mottle virus (SMoV), strawberry crinkle virus (SCV) and strawberry virus 1 (StrV-1). While SCV and StrV-1 are represented by two and three molecular variants, respectively, SmoV has three different RNA1 and RNA2 segments. In this study, we focus on virus acquisition by individual adult aphids of the Aphis gossypii, Aphis forbesi and Chaetosiphon fragaefolii species. Single-aphid transmission trials are performed under experimental conditions. Both different viruses and individual virus strains show varying performances in single aphid acquisition. The obtained data suggests that numerous individual transmission events lead to the establishment of multistrain infections. These data will be important for the development of epidemiological models in plant virology.
Zobrazit více v PubMed
Raccah B., Fereres A. eLS. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2009. Plant Virus Transmission by Insects.
Stobbe A.H., Roossinck M.J. Plant Virus Metagenomics: What We Know and Why We Need to Know More. Front. Plant Sci. 2014;5:150. doi: 10.3389/fpls.2014.00150. PubMed DOI PMC
Maclot F., Candresse T., Filloux D., Malmstrom C.M., Roumagnac P., van der Vlugt R., Massart S. Illuminating an Ecological Blackbox: Using High Throughput Sequencing to Characterize the Plant Virome Across Scales. Front. Microbiol. 2020;11:578064. doi: 10.3389/fmicb.2020.578064. PubMed DOI PMC
Moreno A.B., López-Moya J.J. When Viruses Play Team Sports: Mixed Infections in Plants. Phytopathology. 2020;110:29–48. doi: 10.1094/PHYTO-07-19-0250-FI. PubMed DOI
Syller J. Facilitative and Antagonistic Interactions between Plant Viruses in Mixed Infections: Plant Virus Interactions in Mixed Infections. Mol. Plant Pathol. 2012;13:204–216. doi: 10.1111/j.1364-3703.2011.00734.x. PubMed DOI PMC
Martin V., Domingo E. Influence of the Mutant Spectrum in Viral Evolution: Focused Selection of Antigenic Variants in a Reconstructed Viral Quasispecies. Mol. Biol. Evol. 2008;25:1544–1554. doi: 10.1093/molbev/msn099. PubMed DOI
Roossinck M.J. Origin and Evolution of Viruses. Elsevier; Amsterdam, The Netherlands: 2008. Mutant Clouds and Bottleneck Events in Plant Virus Evolution; pp. 251–258.
Domingo E., Perales C. Viral Quasispecies. PLoS Genet. 2019;15:e1008271. doi: 10.1371/journal.pgen.1008271. PubMed DOI PMC
Maliogka V., Minafra A., Saldarelli P., Ruiz-García A., Glasa M., Katis N., Olmos A. Recent Advances on Detection and Characterization of Fruit Tree Viruses Using High-Throughput Sequencing Technologies. Viruses. 2018;10:436. doi: 10.3390/v10080436. PubMed DOI PMC
Garcia S., Hily J.-M., Komar V., Gertz C., Demangeat G., Lemaire O., Vigne E. Detection of Multiple Variants of Grapevine Fanleaf Virus in Single Xiphinema Index Nematodes. Viruses. 2019;11:1139. doi: 10.3390/v11121139. PubMed DOI PMC
Bergua M., Kang S.-H., Folimonova S.Y. Understanding Superinfection Exclusion by Complex Populations of Citrus Tristeza Virus. Virology. 2016;499:331–339. doi: 10.1016/j.virol.2016.10.001. PubMed DOI
Kleynhans J., Pietersen G. Comparison of Multiple Viral Population Characterization Methods on a Candidate Cross-Protection Citrus Tristeza Virus (CTV) Source. J. Virol. Methods. 2016;237:92–100. doi: 10.1016/j.jviromet.2016.09.003. PubMed DOI
Zhang X.-F., Zhang S., Guo Q., Sun R., Wei T., Qu F. A New Mechanistic Model for Viral Cross Protection and Superinfection Exclusion. Front. Plant Sci. 2018;9:40. doi: 10.3389/fpls.2018.00040. PubMed DOI PMC
Johnson A.M.A., Gopal D.V.R.S., Sudhakar C. GM Crops for Plant Virus Resistance: A Review. In: Kavi Kishor P.B., Rajam M.V., Pullaiah T., editors. Genetically Modified Crops. Springer; Singapore: 2021. pp. 257–337.
Harper S.J., Cowell S.J., Dawson W.O. Bottlenecks and Complementation in the Aphid Transmission of Citrus Tristeza Virus Populations. Arch. Virol. 2018;163:3373–3376. doi: 10.1007/s00705-018-4009-1. PubMed DOI
Piche L.M., Singh R.P., Nie X., Gudmestad N.C. Diversity Among Potato Virus Y Isolates Obtained from Potatoes Grown in the United States. Phytopathology. 2004;94:1368–1375. doi: 10.1094/PHYTO.2004.94.12.1368. PubMed DOI
Della Bartola M., Byrne S., Mullins E. Characterization of Potato Virus Y Isolates and Assessment of Nanopore Sequencing to Detect and Genotype Potato Viruses. Viruses. 2020;12:478. doi: 10.3390/v12040478. PubMed DOI PMC
Ng J.C., Zhou J.S. Insect Vector–Plant Virus Interactions Associated with Non-Circulative, Semi-Persistent Transmission: Current Perspectives and Future Challenges. Curr. Opin. Virol. 2015;15:48–55. doi: 10.1016/j.coviro.2015.07.006. PubMed DOI
Hogenhout S.A., Ammar E.-D., Whitfield A.E., Redinbaugh M.G. Insect Vector Interactions with Persistently Transmitted Viruses. Annu. Rev. Phytopathol. 2008;46:327–359. doi: 10.1146/annurev.phyto.022508.092135. PubMed DOI
Ng J.C.K., Perry K.L. Transmission of Plant Viruses by Aphid Vectors. Mol. Plant Pathol. 2004;5:505–511. doi: 10.1111/j.1364-3703.2004.00240.x. PubMed DOI
Allen L.J.S., Bokil V.A., Cunniffe N.J., Hamelin F.M., Hilker F.M., Jeger M.J. Modelling Vector Transmission and Epidemiology of Co-Infecting Plant Viruses. Viruses. 2019;11:1153. doi: 10.3390/v11121153. PubMed DOI PMC
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
Whitfield A.E., Huot O.B., Martin K.M., Kondo H., Dietzgen R.G. Plant Rhabdoviruses—Their Origins and Vector Interactions. Curr. Opin. Virol. 2018;33:198–207. doi: 10.1016/j.coviro.2018.11.002. PubMed DOI
Gallet R., Michalakis Y., Blanc S. Vector-Transmission of Plant Viruses and Constraints Imposed by Virus–Vector Interactions. Curr. Opin. Virol. 2018;33:144–150. doi: 10.1016/j.coviro.2018.08.005. PubMed DOI
Moury B., Fabre F., Senoussi R. Estimation of the Number of Virus Particles Transmitted by an Insect Vector. Proc. Natl. Acad. Sci. USA. 2007;104:17891–17896. doi: 10.1073/pnas.0702739104. PubMed DOI PMC
Ali A., Li H., Schneider W.L., Sherman D.J., Gray S., Smith D., Roossinck M.J. Analysis of Genetic Bottlenecks during Horizontal Transmission of Cucumber mosaic Virus. J. Virol. 2006;80:8345–8350. doi: 10.1128/JVI.00568-06. PubMed DOI PMC
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
Bragard C., Dehnen-Schmutz K., Gonthier P., Jacques M., Jaques Miret J.A., Justesen A.F., MacLeod A., Magnusson C.S., Milonas P., EFSA Panel on Plant Health (PLH) et al. Pest Categorisation of Non-EU Viruses of Fragaria L. EFSA J. 2019;17:e05766. doi: 10.2903/j.efsa.2019.5766. PubMed DOI PMC
Fránová J., Přibylová J., Koloniuk I. Molecular and Biological Characterization of a New Strawberry Cytorhabdovirus. Viruses. 2019;11:982. doi: 10.3390/v11110982. PubMed DOI PMC
Diaz-Lara A., Stevens K.A., Klaassen V., Hwang M.S., Al Rwahnih M. Sequencing a Strawberry Germplasm Collection Reveals New Viral Genetic Diversity and the Basis for New RT-QPCR Assays. Viruses. 2021;13:1442. doi: 10.3390/v13081442. PubMed DOI PMC
Koloniuk I., Přibylová J., Čmejla R., Valentová L., Fránová J. Identification and Characterization of a Novel Umbra-like Virus, Strawberry Virus A, Infecting Strawberry Plants. Plants. 2022;11:643. doi: 10.3390/plants11050643. PubMed DOI PMC
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
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
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;164:3127–3131. doi: 10.1007/s00705-019-04390-y. PubMed DOI
Dara S.K. Virus Decline of Strawberry in California and the Role of Insect Vectors and Associated Viruses. Plant Health Prog. 2015;16:211–215. doi: 10.1094/PHP-MR-15-0023. 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
Harry M., Solignac M., Lachaise D. Molecular Evidence for Parallel Evolution of Adaptive Syndromes in Fig-Breeding Lissocephala (Drosophilidae) Mol. Phylogenet. Evol. 1998;9:542–551. doi: 10.1006/mpev.1998.0508. 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
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
R Development Core Team . R: A Language and Environment for Statistical Computing. R Core Team; Vienna, Austria: 2014.
Wickham H. Ggplot2: Elegant Graphics for Data Analysis. Springer; New York, NY, USA: 2016.
Koonin E.V., Dolja V.V., Krupovic M., Varsani A., Wolf Y.I., Yutin N., Zerbini F.M., Kuhn J.H. Global Organization and Proposed Megataxonomy of the Virus World. Microbiol. Mol. Biol. Rev. 2020;84:e00061-19. doi: 10.1128/MMBR.00061-19. PubMed DOI PMC
Bruyere A., Wantroba M., Flasinski S., Dzianott A., Bujarski J.J. Frequent Homologous Recombination Events between Molecules of One RNA Component in a Multipartite RNA Virus. J. Virol. 2000;74:4214–4219. doi: 10.1128/JVI.74.9.4214-4219.2000. PubMed DOI PMC
Vives M.C., Rubio L., Sambade A., Mirkov T.E., Moreno P., Guerri J. Evidence of Multiple Recombination Events between Two RNA Sequence Variants within a Citrus Tristeza Virus Isolate. Virology. 2005;331:232–237. doi: 10.1016/j.virol.2004.10.037. PubMed DOI
Payne S. Viruses: From Understanding to Investigation. Elsevier; Amsterdam, The Netherlands: 2017. Virus Evolution and Genetics; pp. 81–86.
Chare E.R., Gould E.A., Holmes E.C. Phylogenetic Analysis Reveals a Low Rate of Homologous Recombination in Negative-Sense RNA Viruses. J. Gen. Virol. 2003;84:2691–2703. doi: 10.1099/vir.0.19277-0. PubMed DOI
Longdon B., Day J.P., Schulz N., Leftwich P.T., de Jong M.A., Breuker C.J., Gibbs M., Obbard D.J., Wilfert L., Smith S.C.L., et al. Vertically Transmitted Rhabdoviruses Are Found across Three Insect Families and Have Dynamic Interactions with Their Hosts. Proc. R. Soc. B Biol. Sci. 2017;284:20162381. doi: 10.1098/rspb.2016.2381. PubMed DOI PMC
Budzyńska D., Minicka J., Hasiów-Jaroszewska B., Elena S.F. Molecular Evolution of Tomato Black Ring Virus and de Novo Generation of a New Type of Defective RNAs during Long-term Passaging in Different Hosts. Plant Pathol. 2020;69:1767–1776. doi: 10.1111/ppa.13258. DOI
Syller J., Grupa A. Antagonistic Within-Host Interactions between Plant Viruses: Molecular Basis and Impact on Viral and Host Fitness: Antagonistic Interactions between Plant Viruses. Mol. Plant Pathol. 2016;17:769–782. doi: 10.1111/mpp.12322. PubMed DOI PMC
Eastop V. Worldwide Importance Of Aphids As Virus Vectors. In: Harris K., Maramorosch K., editors. Aphids as Virus Vectors. Elsevier; New York, NY, USA: 1977. pp. 3–62.
Harper S.J., Cowell S.J., Dawson W.O. Isolate Fitness and Tissue-Tropism Determine Superinfection Success. Virology. 2017;511:222–228. doi: 10.1016/j.virol.2017.08.033. PubMed DOI