Turnip yellows virus (TuYV) is one of the most important pathogens of oilseed rape worldwide. The virus has a large host range including many crop species (e.g., oilseed rape, pea, chickpea) and weeds from more than twenty plant families. Other than oilseed rape, we detected TuYV in many commonly grown weed species that share the fields and vegetation period together with canola crops in Czech and Slovak Republics. TuYV was detected by reverse-transcription polymerase chain reaction (RT-PCR) in at least 26 species including main crop hosts (oilseed rape), intercrops and weeds such as Amaranthus retroflexus, Atriplex patula (Amaranthaceae), Arctium lappa, Lactuca serriola, Taraxacum officinale, Tripleurospermum inodorum (Asteraceae), Phacelia tanacetifolia (Boraginaceae), Brassica napus, Capsella bursa-pastoris, Descurainia Sophia, Raphanus raphanistrum, Sinapis alba, Sisymbrium officinale, Thlaspi arvense (Brassicaceae), Silene alba, Stellaria media (Caryophyllaceae), Euphorbia helioscopia (Euphorbiaceae), Geranium rotundifolium (Geraniaceae), Lamium purpureum (Lamiaceae), Fumaria officinalis, Papaver rhoeas (Papaveraceae), Veronica persica (Plantaginaceae syn. Scrophulariaceae), Fallopia convolvulus (Polygonaceae), Solanum nigrum (Solanaceae), Urtica dioica (Urticaceae) and Viola arvensis (Violaceae). The detection of TuYV was further confirmed by RT-qPCR as well as Sanger sequencing of the PCR fragments. We discovered four new weed species as hosts of TuYV such as T. inodorum, S. alba, G. rotundifolium and E. helioscopia, representing their three respective plant families. The readthrough domain (RTD) gene sequence analysis of the Czech and Slovak TuYV isolates from oilseed rape and weed species showed similar within-group nucleotide divergence (7.1% and 5.6%, respectively) and the absence of geographical- or host-based phylogenetic clustering. The high-throughput sequencing of the P. rhoeas sample enabled the obtention of a nearly complete genome of TuYV and revealed the mixed infection of TuYV with turnip mosaic virus and cucumber mosaic virus. Our results thus show that weed species are an important TuYV reservoir and play a significant role in the spread and incidence of the disease in field crops such as oilseed rape.

Biomedical Research Center of the Slovak Academy of Sciences Institute of Virology Dúbravská Cesta 9 84505 Bratislava Slovakia

Department of Microbiology and Virology Comenius University in Bratislava Ilkovičova 6 84104 Bratislava Slovakia

Department of Plant Protection Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 Prague 16500 Czech Republic

Faculty of Natural Sciences University of Ss Cyril and Methodius Nám J Herdu 2 91701 Trnava Slovakia

Plant Virus and Vector Interactions Crop Research Institute Drnovská 507 Prague 16106 Czech Republic

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Walsh J.A., Tomlinson J.A. Viruses infecting winter oilseed rape (Brassica-napus ssp oleifera) Ann. Appl. Biol. 1985;107:485–495. doi: 10.1111/j.1744-7348.1985.tb03165.x. DOI

Jones R.A.C., Sharman M., Trebicki P., Maina S., Congdon B.S. Virus diseases of cereal and oilseed crops in Australia: Current position and future challenges. Viruses. 2021;13:2051. doi: 10.3390/v13102051. PubMed DOI PMC

Hardwick N.V., Davies J.M.L., Wright D.M. The incidence of three diseases of winter oilseed rape in England and Wales in the 1991/92 and 1992/93 growing season. Plant Pathol. 1994;43:1045–1049. doi: 10.1111/j.1365-3059.1994.tb01656.x. DOI

Duffus J.E. Host relationship of beet western yellows virus strains. Phytopathology. 1964;54:736–738.

Graichen K., Rabenstein F. European isolates of Beet western yellows virus (BWYV) from oilseed rape (Brassica napus L. ssp. napus) are non-pathogenic on sugar beet (Beta vulgaris L. var. altissima) but represent isolates of Turnip yellows virus (TuYV) J. Plant Dis. Prot. 1996;103:233–245.

Wallis R.L. Some host plants of the green peach aphid and beet western yellows virus in the Pacific Northwest. J. Econ. Entomol. 1967;60:904–907. doi: 10.1093/jee/60.4.904. DOI

Goyal G., Harsimran K.G., McSorley R. Common Weed Hosts of Insect-Transmitted Viruses of Florida Vegetable Crops. University of Florida Institute of Food and Agricultural Sciences; Gainesville, FL, USA: 2022. [(accessed on 29 April 2022)]. ENY-863. Available online: https://edis.ifas.ufl.edu/publication/in931.

Stevens M., Smith H.G., Hallsworth P.B. The host-range of Beet yellowing viruses among common arable weed species. Plant Pathol. 1994;43:579–588. doi: 10.1111/j.1365-3059.1994.tb01593.x. DOI

Stevens M., McGrann G., Clark B., Authority H. Turnip yellows virus (syn Beet western yellows virus): An emerging threat to European oilseed rape production? HGCA Res. Rev. 2008;69:1–37.

Freeman A., Aftab M. Effective management of viruses in pulse crops in south eastern Australia should include management of weeds. Australas. Plant Pathol. 2011;40:430–441. doi: 10.1007/s13313-011-0058-6. DOI

Chalupníková J., Kundu J.K., Singh K., Bartakova P., Beoni E. Wheat streak mosaic virus: Incidence in field crops, potential reservoir within grass species and uptake in winter wheat cultivars. J. Integr. Agric. 2017;16:523–531. doi: 10.1016/S2095-3119(16)61486-7. DOI

Rashidi M., Cruzado K.R., Hutchinson S.J.P., Bosque-Pérez A.N., Marshall M.J., Rashed A. Grassy weeds and corn as potential sources of barley yellow dwarf virus spread into winter wheat. Plant Dis. 2021;105:444–449. doi: 10.1094/PDIS-05-20-1004-RE. PubMed DOI

Yazdkhasti E., Hopkins J.R., Kvarnheden A. Reservoirs of plant virus disease: Occurrence of wheat dwarf virus and barley/cereal yellow dwarf viruses in Sweden. Plant Pathol. 2021;70:1552–1561. doi: 10.1111/ppa.13414. DOI

Souza T.A., Macedo M.A., Albuquerque L.C., Inoue-Nagata K.A. Host range and natural infection of tomato chlorosis virus in weeds collected in Central Brazil. Trop. Plant Pathol. 2020;45:84–90. doi: 10.1007/s40858-019-00323-x. DOI

Korbecka-Glinka G., Przyby´s M., Feledyn-Szewczyk B.A. Survey of five plant viruses in weeds and tobacco in Poland. Agronomy. 2021;11:1667. doi: 10.3390/agronomy11081667. DOI

Hancinsky R., Mihalik D., Mrkvova M., Candresse T., Glasa M. Plant viruses infecting Solanaceae family members in the cultivated and wild environments: A review. Plants. 2020;9:667. doi: 10.3390/plants9050667. PubMed DOI PMC

Maliano M.R., Macedo M.A., Rojas M.R., Gilbertson R.L. Weed-infecting viruses in a tropical agroecosystem present different threats to crops and evolutionary histories. PLoS ONE. 2021;16:e0250066. doi: 10.1371/journal.pone.0250066. PubMed DOI PMC

Chen G., Pan H., Xie W., Wang S., Wu Q., Fang Y., Shi X., Zhang Y. Virus infection of a weed increases vector attraction to and vector fitness on the weed. Sci. Rep. 2013;3:2253. doi: 10.1038/srep02253. PubMed DOI PMC

Sõmera M., Fargette D., Hébrard E., Sarmiento C. ICTV Report Consortium: ICTV Virus Taxonomy Profile: Solemoviridae. J. Gen. Virol. 2021;102:001707. PubMed PMC

Stevens M., Freeman B., Liu H.Y., Herrbach E., Lemaire O. Beet poleroviruses: Close friends or distant relatives? Mol. Plant Pathol. 2005;6:1–9. doi: 10.1111/j.1364-3703.2004.00258.x. PubMed DOI

Pfeffer S., Dunoyer P., Heim F., Richards K.E., Jonard G., Ziegler-Graff V. P0 of Beet western yellows virus is a suppressor of posttranscriptional gene silencing. J. Virol. 2002;76:6815–6824. doi: 10.1128/JVI.76.13.6815-6824.2002. PubMed DOI PMC

Bortolamiol D., Pazhouhandeh M., Marrocco K., Genschik P., Ziegler-Graff V. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 2007;17:1615–1621. doi: 10.1016/j.cub.2007.07.061. PubMed DOI

Reutenauer A., Ziegler-Graff V., Lot H., Scheidecker D., Guilley H., Richards K., Jonard G. Identification of Beet western yellows virus luteovirus genes implicated in viral replication and particle morphogenesis. Virology. 1993;195:692–699. doi: 10.1006/viro.1993.1420. PubMed DOI

Martin R.R., Keese P.K., Young M.J., Waterhouse P.M., Gerlach W.L. Evolution and molecular biology of luteoviruses. Annu. Rev. Phytopathol. 1990;28:341–363. doi: 10.1146/annurev.py.28.090190.002013. DOI

Brault V., van den Heuvel J.F., Verbeek M., Ziegler-Graff V., Reutenauer A., Herrbach E., Garaud J.C., Guilley H., Richards K., Jonard G. Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J. 1995;14:650–659. doi: 10.1002/j.1460-2075.1995.tb07043.x. PubMed DOI PMC

Van den Heuvel J.F.J.M., Bruyère A., Hogenhout A., Ziegler-Graff V., Brault V., Verbeek M., van der Wilk F., Richards K. The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J. Virol. 1997;71:7258–7265. doi: 10.1128/jvi.71.10.7258-7265.1997. PubMed DOI PMC

Peter K.A., Gildow F., Palukaitis P., Gray S.M. The C terminus of the polerovirus P5 readthrough domain limits virus infection to the phloem. J. Virol. 2009;83:5419–5429. doi: 10.1128/JVI.02312-08. PubMed DOI PMC

Smirnova E., Firth A.E., Miller W.A., Scheidecker D., Brault V., Reinbold C., Rakotondrafara A.M., Chung B.Y.W., Ziegler-Graff V. Discovery of a small non-AUG-initiated ORF in poleroviruses and luteoviruses that is required for long-distance movement. PLoS Pathog. 2015;11:e1004868. doi: 10.1371/journal.ppat.1004868. PubMed DOI PMC

Filardo F., Nancarrow N., Kehoe M., McTaggart A.R., Congdon B., Kumari S., Aftab M., Trębicki P., Rodoni B., Thomas J., et al. Genetic diversity and recombination between turnip yellows virus strains in Australia. Arch. Virol. 2021;166:813–829. doi: 10.1007/s00705-020-04931-w. PubMed DOI

Brault V., Périgon S., Reinbold C., Erdinger M., Scheidecker D., Herrbach E., Richards K., Ziegler-Graff V. The polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid. J. Virol. 2005;79:9685–9693. doi: 10.1128/JVI.79.15.9685-9693.2005. PubMed DOI PMC

Hanzlik K., Gerowitt B. Occurrence and distribution of important weed species in German winter oilseed rape fields. J. Plant Dis. Prot. 2012;119:107–120. doi: 10.1007/BF03356429. DOI

Krähmer H., Andreasen C., Economou-Antonaka G., Holec J., Kalivas D., Kolářová M., Novák R., Panozzog S., Pinke G., Salonen J., et al. Weed surveys and weed mapping in Europe: State of the art and future tasks. Crop Prot. 2020;129:105010. doi: 10.1016/j.cropro.2019.105010. DOI

Abraham A.D., Menzel W., Lesemann D.E., Varrelmann M., Vetten H.J. Chickpea chlorotic stunt virus: A new polerovirus infecting cool-season food legumes in ethiopia. Phytopathology. 2006;96:437–446. doi: 10.1094/PHYTO-96-0437. PubMed DOI

Singh K., Slavíková L., Kumar J. Reakční Směs pro Kvantifikaci Viru Žloutenky Vodnice v Kulturních a Nekulturních Vzorcích Pomocí qPCR (Reaction Mixture for Quantification of Turnip Yellows Virus in Cultivated and Uncultivated Plant Samples by qPCR) Industrial Property Office; Prague, Czech Republic: 2021. Užitný Vzor (Utility Model) no. 35269.

Jarošová J., Kundu J.K. Validation of reference genes as internal control for studying viral infections in cereals by quantitative real-time RT-PCR. BMC Plant Biol. 2010;10:146. doi: 10.1186/1471-2229-10-146. PubMed DOI PMC

Dráb T., Svobodová E., Ripl J., Jarošová J., Rabenstein F., Melcher U., Kundu J.K. SYBR Green I based RT-qPCR assays for the detection of RNA viruses of cereals and grasses. Crop Pasture Sci. 2014;65:1323–1328. doi: 10.1071/CP14151. DOI

Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948. doi: 10.1093/bioinformatics/btm404. PubMed DOI

Kumar S., Stecher G., Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Librado P., Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI

Walkey D.G.A., Pink D.A.C. Studies on resistance to Beet western yellows virus in lettuce (Lactuca sativa) and the occurrence of field sources of the virus. Plant Pathol. 1990;39:141–155. doi: 10.1111/j.1365-3059.1990.tb02485.x. DOI

Pallett D.W., Thurston M.I., Cortina-Borja M., Edwards M.L., Alexander M., Mitchell E., Raybould A.F., Cooper J.I. The incidence of viruses in wild Brassica rapa ssp. sylvestris in southern England. Ann. Appl. Biol. 2002;141:163–170. doi: 10.1111/j.1744-7348.2002.tb00209.x. DOI

Thurston M.I., Pallett D.W., Cortina-Borja M., Edwards M.L., Raybould A.F., Cooper J.I. The incidence of viruses in wild Brassica nigra in Dorset (UK) Ann. Appl. Biol. 2001;139:277–284. doi: 10.1111/j.1744-7348.2001.tb00140.x. DOI

Coutts B.A., Hawkes J.R., Jones R.A.C. Occurrence of Beet western yellows virus and its aphid vectors in over-summering broad-leafed weeds and volunteer crop plants in the grainbelt region of south-western Australia. Aust. J. Agric. Res. 2006;57:975–982. doi: 10.1071/AR05407. DOI

Kolářová M., Tyšer J., Soukup J. Survey about the weed occurrence on arable land in the Czech Republic. Sci. Agric. Bohem. 2013;44:63–69. doi: 10.7160/sab.2013.440210. DOI

Jursík M., Holec J., Soukup J., Venclová V. Competitive relationships between sugar beet and weeds in dependence on time of weed control. Plant Soil Environ. 2008;54:108–116. doi: 10.17221/2687-PSE. DOI

Latham L.J., Smith L.J., Jones R.A.C. Incidence of three viruses in vegetable brassica plantings and associated wild radish weeds in south-west Australia. Australas. Plant Pathol. 2003;32:387–391. doi: 10.1071/AP03031. DOI

Primot S., Valantin-Morison M., Makowski D. Predicting the risk of weed infestation in winter oilseed rape crops. Weed Res. 2005;46:22–33. doi: 10.1111/j.1365-3180.2006.00489.x. DOI

Maree H.J., Fox A., Al Rwahnih M., Boonham N., Candresse T. Application of HTS for routine plant virus diagnostics: State of the art and challenges. Front. Plant Sci. 2018;9:1082. doi: 10.3389/fpls.2018.01082. PubMed DOI PMC

Mrkvová M., Hančinský R., Predajňa L., Alaxin P., Achs A., Tomašechová J., Šoltys K., Mihálik D., Olmos A., Ruiz-García A.B., et al. High-throughput sequencing discloses the Cucumber mosaic virus (CMV) diversity in Slovakia and reveals new hosts of CMV from the Papaveraceae family. Plants. 2022;11:1665. doi: 10.3390/plants11131665. PubMed DOI PMC

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