Raspberry (Rubus idaeus L.) is susceptible to aphid-borne viruses. We studied the incidence of four of them - black raspberry necrosis virus (BRNV), raspberry leaf mottle virus (RLMV), raspberry vein chlorosis virus (RVCV), and Rubus yellow net virus (RYNV) - in raspberry plants and aphids in and around Norwegian raspberry crops for three years (2019, 2021, and 2022). Most of the samples were from symptomatic plants. Applying RT-PCR, 274 leaf samples and 107 aphid samples were analyzed. All four viruses were found, but BRNV dominated: it was detected in 93% of the 178 leaf samples with virus and was the only virus that occurred more frequently as a single infection than in co-infections with the other viruses. The old cv. Veten had the highest virus incidence (97%) among the sampled plants, followed by uncultivated raspberry in the boundary vegetation (82%). All aphids identified were Amphorophora idaei and Aphis idaei. BRNV and/or RLMV was detected in 27% of the aphid samples. Notably, BRNV was detected in 30% of A. idaei samples, a species not known as a BRNV vector. In subsequent transmission experiments we found that although A. idaei can acquire BRNV within one hour, it did not transmit the virus to healthy raspberry plants. In contrast, Am. idaei, a known BRNV vector, was able to acquire the virus within one minute and transmit it within one hour of inoculation. Our study will improve the identification and management of BRNV.

Biology Centre CAS Institute of Plant Molecular Biology České Budějovice Czechia

Division of Biotechnology and Plant Health Norwegian Institute of Bioeconomy Research Ås Norway

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Abhinash B., Shreya K., Markad Ajinkya B., Meenakshi R., Seweta S. (2023). Mechanism of arthropod-mediated transmission of plant viruses - A review. J. Advanced Zoology 44, 38–52. doi: 10.17762/jaz.v44is6.1960 DOI

Alford D. V. (2007). Pests of fruit crops: a color handbook (London, UK: Elsevier; ).

Bettoni J. C., Wang M. R., Li J. W., Fan X., Fazio G., Hurtado-Gonzales O. P., et al. . (2024). Application of biotechniques for in vitro virus and viroid elimination in pome fruit crops. Phytopathology 114, 930–954. doi: 10.1094/PHYTO-07-23-0232-KC PubMed DOI

Blackman R., Eastop V., Hills M. (1977). Morphological and cytological separation of Amphorophora Buckton (Homoptera: Aphididae) feeding on European raspberry and blackberry (Rubus spp.). Bull. Entomological Res. 67, 285–296. doi: 10.1017/S000748530001110X DOI

Blackman R. L., Eastop V. F. (2000). Aphids on the world's crops: an identification and information guide. Second Edition. (West Sussex, England: John Wiley & Sons Ltd; ). 466 pp.

Börner C. (1939). Neue Gattungen und Arten der mitteleuropäischen Aphidenfauna. Arbeiten über physiologische und angewandte Entomologie aus Berlin-Dahlem 6 (1), 75–83.

Bøthun M., Heiberg N. (2004). Satsing på økologisk bringebær (Production of organic raspberries in Norway). Norsk Frukt og bær 7, 16–18.

Converse R. H. (1963). Influence of heat-labile components of the raspberry mosaic complex on growth and yield of red raspberries. Phytopathology 53, 1.

Converse R. H. (1987). Virus diseases of small fruits. USDA Agricultural Handbook No 631. 277 ss. Washington D.C., USA.

Dietzgen R., Mann K., Johnson K. (2016). Plant virus–insect vector interactions: current and potential future research directions. Viruses 8, 303. doi: 10.3390/v8110303 PubMed DOI PMC

FAO (2022). FAOSTAT statistical database (Rome: Food and Agriculture Organisation of the United Nations; ).

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. (1994). DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechno. 3 (5), 294–9. PubMed

Fotirić Akšić M., Nešović M., Ćirić I., Tešić Ž., Pezo L., Tosti T., et al. . (2022). Chemical fruit profiles of different raspberry cultivars grown in specific Norwegian agroclimatic conditions. Horticulturae 8, 765. doi: 10.3390/horticulturae8090765 DOI

Freeman J., Stace-Smith R. (1970). Effects of raspberry mosaic viruses on yield and growth of red raspberries. Can. J. Plant Sci. 50, 521–527. doi: 10.4141/cjps70-099 DOI

Gordon S., Woodford J., Birch A. (1997). Arthropod pests of Rubus in Europe: pest status, current and future control strategies. J. Hortic. Sci. 72, 831–862. doi: 10.1080/14620316.1997.11515577 DOI

Haffner K., Rosenfeld H. J., Skrede G., Wang L. (2002). Quality of red raspberry Rubus idaeus L. cultivars after storage in controlled and normal atmospheres. Postharvest Biol. Technol. 24, 279–289. doi: 10.1016/S0925-5214(01)00147-8 DOI

Halgren A., Tzanetakis I. E., Martin R. R. (2007). Identification, Characterization, and Detection of Black raspberry necrosis virus. Phytopathology® 97, 44–50. doi: 10.1094/phyto-97-0044 PubMed DOI

Heiberg N., Standal R., Måge F. (2002). Evaluation of red raspberry cultivars in Norway. Acta Hortic. 585, 199–202. doi: 10.17660/ActaHortic.2002.585.31 DOI

Jones A., Jennings D. (1980). Genetic control of the reactions of raspberry to black raspberry necrosis, raspberry leaf mottle and raspberry leaf spot viruses. Ann. Appl. Biol. 96, 59–65. doi: 10.1111/j.1744-7348.1980.tb04769.x DOI

Jones A. T., McGavin W. J., Geering A. D. W., Lockhart B. E. L. (2002). Identification of Rubus yellow net virus as a distinct badnavirus and its detection by PCR in Rubus species and in aphids. Ann. Appl. Biol. 141, 1–10. doi: 10.1111/j.1744-7348.2002.tb00189.x DOI

Jones S., McGavin W., MacFarlane S. (2019). The complete sequences of two divergent variants of the rhabdovirus raspberry vein chlorosis virus and the design of improved primers for virus detection. Virus Res. 265, 162–165. doi: 10.1016/j.virusres.2019.03.004 PubMed DOI

Koloniuk I., Fránová J., Přibylová J., Sarkisova T., Špak J., Tan J. L., et al. . (2023). Molecular characterization of a novel enamovirus infecting raspberry. Viruses 15, 2281. doi: 10.3390/v15122281 PubMed DOI PMC

Lenz O., Koloniuk I., Sarkisová T., Čmejla R., Valentová L., Rejlová M., et al. . (2024). Molecular characterization of a novel rubodvirus infecting raspberries. Viruses 16, 1074. doi: 10.3390/v16071074 PubMed DOI PMC

Lightle D. M., Dossett M., Backus E. A., Lee J. C. (2012). Location of the mechanism of resistance to Amphorophora agathonica (Hemiptera: Aphididae) in red raspberry. J. Economic Entomology 105, 1465–1470. doi: 10.1603/ec11405 PubMed DOI

Martin R. R., MacFarlane S., Sabanadzovic S., Quito D., Poudel B., Tzanetakis I. E. (2013). Viruses and virus diseases of Rubus. Plant Dis. 97, 168–182. doi: 10.1094/PDIS-04-12-0362-FE PubMed DOI

McGavin W., McMenemy L., MacFarlane S. (2010). The complete sequence of a UK strain of black raspberry necrosis virus. Arch. Virol. 155, 1897–1899. doi: 10.1007/s00705-010-0807-9 PubMed DOI

McMenemy L. S., Hartley S. E., MacFarlane S. A., Karley A. J., Shepherd T., Johnson S. N. (2012). Raspberry viruses manipulate the behaviour of their insect vectors. Entomologia Experimentalis Applicata 144, 56–68. doi: 10.1111/j.1570-7458.2012.01248.x DOI

McMenemy L. S., Mitchell C., Johnson S. N. (2009). ). Biology of the European large raspberry aphid, Amphorophora idaei: its role in virus transmission and resistance breakdown in red raspberry. Agric. For. Entomology 11, 61–71. doi: 10.1111/j.1461-9563.2008.00409.x DOI

Menzel W., Jelkmann W., Maiss E. (2002). Detection of four apple viruses by multiplex RT-PCR assays with coamplification of plant mRNA as internal control. J. Virological Methods 99, 81–92. doi: 10.1016/S0166-0934(01)00381-0 PubMed DOI

Stace-Smith R. (1955. a). Studies on rubus virus diseases in British Columbia: i. rubus yellow-net. Can. J. Bot. 33, 269–274. doi: 10.1139/b55-020 DOI

Stace-Smith R. (1955. b). Studies on Rubus Virus Diseases in British Columbia: II. Black raspberry necrosis. Can. J. Bot. 33, 314–322. doi: 10.1139/b55-027 DOI

Stace-Smith R. (1961). Studies on rubus virus diseases in British Columbia: vii. raspberry vein chlorosis. Can. J. Bot. 39, 559–565. doi: 10.1139/b61-045 DOI

Susi H., Rajamäki M. L., Artola K., Jayaraj-Mallika F. R., Valkonen J. P. T. (2018). Molecular detection and characterisation of black raspberry necrosis virus and raspberry bushy dwarf virus isolates in wild raspberries. Ann. Appl. Biol. 173, 97–111. doi: 10.1111/aab.12438 DOI

Tan J. L., Trandem N., Fránová J., Hamborg Z., Blystad D.-R., Zemek R. (2022). Known and potential invertebrate vectors of raspberry viruses. Viruses 14, 571. doi: 10.3390/v14030571 PubMed DOI PMC

Tatineni S., Hein G. L. (2023). Plant viruses of agricultural importance: current and future perspectives of virus disease management strategies. Phytopathology® 113, 117–141. doi: 10.1094/phyto-05-22-0167-rvw PubMed DOI

Trandem N., Eklo T., Vintland A. (2015). Stor bringebærbladlus (Amphorophora idaei) oppdaget i ‘Glen Ample’. (Large European raspberry aphid discovered in 'Glen Ample'). Norsk Frukt og Bær 18, 13.

Tzanetakis I. E., Halgren A., Mosier N., Martin R. R. (2007). Identification and characterization of Raspberry mottle virus, a novel member of the Closteroviridae. Virus Res. 127, 26–33. doi: 10.1016/j.virusres.2007.03.010 PubMed DOI

Wang M. R., Bi W. L., Bettoni J. C., Zhang D., Volk G. M., Wang Q. C. (2022. a). Shoot tip cryotherapy for plant pathogen eradication. Plant Pathol. 71, 1241–1254. doi: 10.1111/ppa.13565 DOI

Wang M. R., Hamborg Z., Ma X. Y., Blystad D. R., Wang Q. C. (2022. b). Double-edged effects of the cryogenic technique for virus eradication and preservation in shallot shoot tips. Plant Pathol. 71, 494–504. doi: 10.1111/ppa.13466 DOI