Abstract
The most effective management strategy for tomato spotted wilt orthotospovirus (TSWV) has been the use of resistant tomato (Sw-5b+) cultivars. Unfortunately, resistance-breaking isolates (RB) have emerged in many countries. In 2019, TSWV-like symptoms were observed in protected crops of a tomato (Sw-5b+) cultivar in two separate locations in Serbia. To identify variations associated with Serbian TSWV isolates that are able to infect resistant tomato cultivars, 11 samples with TSWV-like symptoms collected from susceptible (Sw-5b−) cultivars from 2011 to 2015, and three collected from the resistant cultivar in 2019 were tested. The presence of TSWV was confirmed serologically in all tomato samples, and partial nucleotide sequences of the NSm and N genes of 14 selected isolates were obtained. The NSm amino acid sequence comparison revealed the presence of two amino acid substitutions (C118Y or T120N) in three isolates originating from tomato (Sw-5b+) indicating their RB phenotype and independent evolutionary events. Isolates originating from tomato (Sw-5b−) cultivars were determined as resistance-inducing isolates (RI). NSm and N gene phylogenetic analyses showed the clustering of Serbian RB and RI isolates regardless of their phenotype. The N gene tree also showed the clustering of Serbian TSWV isolates in different subpopulations within the European clade indicating two independent introduction events and gene flow between southern and northern regions of the country. Bioassay confirmed that three RB isolates had the ability to break the Sw-5b-mediated resistance in tomato, but were unable to overcome the Tsw resistance gene in pepper. This first detection of the Sw-5b resistance-breaking in Serbia shows the necessity of further monitoring to prevent the establishment of RB TSWV isolates.
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References
Almási A, Csilléry G, Csömör Z, Nemes K, Palkovics L, Salanáki K, Tóbiás I (2015) Phylogenetic analysis of Tomato spotted wilt virus (TSWV) NSs protein demonstrates the isolated emergence of resistance-breaking strains in pepper. Virus Genes 50:71–78. https://doi.org/10.1007/s11262-014-1131-3
Aramburu J, Martí M (2003) The occurrence in north-east Spain of a variant of Tomato spotted wilt virus (TSWV) that breaks resistance in tomato (Lycopersicon esculentum) containing the Sw-5 gene. Plant Pathol 52:407. https://doi.org/10.1046/j.1365-3059.2003.00829.x
Aramburu J, Galipienso L, Soler S, López C (2010) Characterization of Tomato spotted wilt virus isolates that overcome the Sw-5 resistance gene in tomato and fitness assays. Phytopathol Mediterr 49: 342–351. https://doi.org/10.14601/Phytopathol_Mediterr-8435
Batuman O, Turini TA, Oliveira PV, Rojas MR, Macedo M, Mellinger HC, Adkins S, Gilbertson RL (2017) First report of a resistance-breaking strain of Tomato spotted wilt virus infecting tomatoes with the Sw-5 Tospovirus-resistance gene in California. Plant Dis 101:637. https://doi.org/10.1094/PDIS-09-16-1371-PDN
Boiteux LS (1995) Allelic relationships between genes for resistance to tomato spotted wilt Tospovirus in Capsicum chinense. Theor Appl Genet 90:146–149. https://doi.org/10.1007/BF00221009
Boiteux LS, Nagata T (1993) Susceptibility in Capsicum chinense PI 159236 to Tomato spotted wilt virus isolates in Brazil. Plant Dis 77:210. https://doi.org/10.1094/PD-77-0210F
Cho JJ, Custer DM, Brommonschenkel SH, Tanksley SD (1996) Conventional breeding: Host-Plant resistance and the use of molecular markers to develop resistance to tomato spotted wilt virus in vegetables. Acta Hortic 431:367–378. https://doi.org/10.17660/ActaHortic.1996.431.31
Ciuffo M, Finetti-Sialer MM, Gallitelli D, Turina M (2005) First report in Italy of a resistance-breaking strain of Tomato spotted wilt virus infecting tomato cultivars carrying the Sw5 resistance gene. Plant Pathol 54:564. https://doi.org/10.1111/j.1365-3059.2005.01203.x
Crescenzi A, Fanigliulo A, Viggiano A (2015) Resistance breaking Tomato spotted wilt virus isolates on resistant tomato cultivars in Italy. Acta Hortic 1069:95–98
de Haan P, Kormelink R, de Oliveira RR, van Poelwijk F, Peters D, Goldbach R (1991) Tomato spotted wilt virus L RNA encodes a putative RNA polymerase. J Gen Virol 72:2207–2216. https://doi.org/10.1099/0022-1317-72-9-2207
de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R,
de Ronde D, Butterbach P, Lohuis D, Hedil M, Van Lent JWM, Kormelink R (2013) Tsw gene-based resistance is triggered by a functional RNA silencing suppressor protein of the Tomato spotted wilt virus. Mol Plant Pathol 14:405–415. https://doi.org/10.1111/mpp.12016
de Ronde D, Pasquier A, Ying S, Butterbach P, Lohuis D, Kormelink R (2014) Analysis of Tomato spotted wilt virus NSs protein indicates the importance of the N-terminal domain for avirulence and RNA silencing suppression. Mol Plant Pathol 15:185–195. https://doi.org/10.1111/mpp.12082
Debreczeni DE, López C, Aramburu J, Darós JA, Soler S, Galipienso L, Falk BW, Rubio L (2015) Complete sequence of three different biotypes of tomato spotted wilt virus (wild type, tomato Sw-5 resistance-breaking and pepper Tsw resistance-breaking) from Spain. Arch Virol 160:2117–2123. https://doi.org/10.1007/s00705-015-2453-8
Deligoz I, Arli Sokmen M, Sari S (2014) First report of resistance breaking strain of Tomato spotted wilt virus (Tospovirus; Bunyaviridae) on resistant sweet pepper cultivars in Turkey. New Dis Rep 30:26. https://doi.org/10.5197/j.2044-0588.2014.030.026
di Rienzo V, Bubici G, Montemurro C, Cillo F (2018) Rapid identification of tomato Sw-5 resistance-breaking isolates of Tomato spotted wilt virus using high resolution melting and TaqMan SNP Genotyping assays as allelic discrimination techniques. PLoS ONE 13:e0196738. https://doi.org/10.1371/journal.pone.0196738
EFSA Panel on Plant Health (PLH) (2012) Scientific opinion on the pest categorization of the tospoviruses. EFSA J 10:2772. https://doi.org/10.2903/j.efsa.2012.2772
Espinosa PJ, Bielza P, Contreras J, Lacasa A (2002) Field and laboratory selection of Frankliniella occidentalis (Pergande) for resistance to insecticides. Pest Manag Sci 58:920–927. https://doi.org/10.1002/ps.573
Ferrand L, Almeida MMS, Orílio AF, Dal Bó E, Resende RO, García ML (2019) Biological and molecular characterization of tomato spotted wilt virus (TSWV) resistance-breaking isolates from Argentina. Plant Pathol 68:1587–1601. https://doi.org/10.1111/ppa.13087
Goldbach R, Peters D (1996) Molecular and biological aspects of tospoviruses. In: Elliot RM (ed) The Bunyaviridae. Plenum Press, New York, pp 129–157
Gordillo LF, Stevens MR, Millard MA, Geary B (2008) Screening two Lycopersicon peruvianum collections for resistance to Tomato spotted wilt virus. Plant Dis 92:694–704. https://doi.org/10.1094/PDIS-92-5-0694
Hallwass M, de Oliveira AS, de Campos DE, Lohuis D, Silva Boiteux L, Kayuko Inoue-Nagata A, Resende RO, Kormelink R (2014) The Tomato spotted wilt virus cell-to-cell movement protein (NSm) triggers a hypersensitive response in Sw-5-containing resistant tomato lines and in Nicotiana benthamiana transformed with the functional Sw-5b resistance gene copy. Mol Plant Pathol 15:871–880. https://doi.org/10.1111/mpp.12144
Hoffmann K, Qiu WP, Moyer JW (2001) Overcoming host- and pathogen-mediated resistance in tomato and tobacco maps to the M RNA of Tomato spotted wilt virus. Mol Plant Microbe in 14:242–249. https://doi.org/10.1094/MPMI.2001.14.2.242
Houle JL, Kennedy GG (2017) Tomato spotted wilt virus can infect resistant Tomato when Western flower thrips inoculate blossoms. Plan Dis 101:1666–1670. https://doi.org/10.1094/PDIS-12-16-1716-RE
Jiang L, Huang Y, Suna L, Wang B, Zhu M, Li J, Huang C, Liu Y, Dong J, Zhang Z, Tao X (2017) Occurrence and diversity of Tomato spotted wilt virus isolates breaking the Tsw resistance gene of Capsicum chinense in Yunnan, southwest China. Plant Pathol 66:980–989. https://doi.org/10.1111/ppa.12645
Jones DR (2005) Plant viruses transmitted by thrips. Eur J Plant Pathol 113:119–157. https://doi.org/10.1007/s10658-005-2334-1
Jović J, Mitrović M, Cvrković T, Krstić O, Toševski I (2012) Occurrence and molecular identification of western flower thrips, Frankliniella occidentalis (Pergande), in Serbia. In: Proceedings of International Symposium „Current Trends in Plant Protection“, Semptember 25–28, Belgrade, Serbia, pp 520–525
Kormelink R (2011) The molecular biology of tospoviruses and resistance strategies. In: Elliott RM, Plyusin A (eds) Bunyaviridae: molecular and cellular biology. Plenum Press, New York, pp 163–191
Krstić B, Bulajić A (2007) Quarantine viruses in protected vegetable and ornamental crops. University of Belgrade-Faculty of Agriculture and Ministry of Agriculture, Forestry, and Water Management of Serbia, Belgrade (in Serbian)
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Latham LJ, Jones RAC (1998) Selection of resistance breaking strains of Tomato spotted wilt tospovirus. Ann Appl Biol 133:385–402. https://doi.org/10.1111/j.1744-7348.1998.tb05838.x
Li R, Mock R, Huang Q, Abad J, Hartung J, Kinard G (2008) A reliable and inexpensive method of nucleic acid extraction for the PCR-based detection of diverse plant pathogens. J Virol Methods 154:48–55. https://doi.org/10.1016/j.jviromet.2008.09.008
López C, Aramburu J, Galipienso L, Soler S, Nuez F, Rubio L (2011) Evolutionary analysis of tomato Sw-5 resistance-breaking isolates of Tomato spotted wilt virus. J Gen Virol 92:210–215. https://doi.org/10.1099/vir.0.026708-0
Margaria P, Ciuffo M, Pacifico D, Turina M (2007) Evidence that the nonstructural protein of tomato spotted wilt virus is the avirulence determinant in the interaction with resistant pepper carrying the Tsw gene. Mol Plant Microbe Interact 20:547–558. https://doi.org/10.1094/MPMI-20-5-0547
Mickovski J (1969) Tomato spotted wilt virus on tobacco in Yugoslavia (Lycopersicum virus 3–Smith). Plant Prot 105:203–214 ((in Serbian))
Nachappa P, Challacombe J, Margolies DC, Nechols JR, Whitfield AE, Rotenberg D (2020) Tomato spotted wilt virus benefits its thrips vector by modulating metabolic and plant defense pathways in Tomato. Front Plant Sci. https://doi.org/10.3389/fpls.2020.575564
Nikolić D, Milojević K, Stanković I, Vučurović A, Ristić D, Bulajić A, Krstić B (2013a) Tomato viruses in Serbia. In: Proceedings of XII Plant protection symposium, November 25–29, Zlatibor, Serbia, pp 44–45 (in Serbian)
Nikolić D, Stanković I, Vučurović A, Ristić D, Milojević K, Bulajić A, Krstić B (2013b) First report of Tomato spotted wilt virus on Brugmansia sp. in Serbia. Plant Dis 97:850. https://doi.org/10.1094/PDIS-10-12-0937-PDN
Nikolić D, Vučurović A, Stanković I, Radović N, Zečević K, Bulajić A, Krstić B (2018) Viruses affecting tomato crops in Serbia. Eur J Plant Pathol 152:225–235. https://doi.org/10.1007/s10658-018-1467-y
OEPP/EPPO (2020) EPPO A2 List. http://www.eppo.org/QUARANTINE/quarantine.htm. 2020
Pappu H, Pappu S, Jain R, Bertrand P, Culbreath A, McPherson R, Csinos A (1998) Sequence characteristics of natural populations of Tomato spotted wilt tospovirus infecting flue-cured tobacco in Georgia. Virus Genes 17:169–177. https://doi.org/10.1023/a:1008072825152
Pappu HR, Jones RAC, Jain RK (2009) Global status of tospovirus epidemics in diverse cropping systems: successes gained and challenges ahead. Virus Res 141:219–236. https://doi.org/10.1016/j.virusres.2009.01.009
Peiró A, Cañizares MC, Rubio L, López C, Moriones E, Aramburu J, Sánchez-Navarro J (2014) The movement protein (NSm) of Tomato spotted wilt virus is the avirulence determinant in the tomato Sw-5 gene-based resistance. Mol Plant Pathol 15:802–813. https://doi.org/10.1111/mpp.12142
Qiu WP, Geske SM, Hickey CM, Moyer JW (1998) Tomato spotted wilt tospovirus genome reassortment and genome segment-specific adaptation. Virology 244:186–194. https://doi.org/10.1006/viro.1998.9131
Roggero P, Masenga V, Tavella L (2002) Field isolates of tomato spotted wilt virus overcoming resistance in pepper and their spread to other hosts in Italy. Plant Dis 86:950–954. https://doi.org/10.1094/PDIS.2002.86.9.950
Roselló S, José Díez M, Nuez F (1996) Viral diseases causing the greatest economic losses to the tomato crop. I. The Tomato spotted wilt virus - a review. Sci Hortic 67:117–150. https://doi.org/10.1016/S0304-4238(96)00946-6
Scholthof KG, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954. https://doi.org/10.1111/j.1364-3703.2011.00752.x
Stanković I, Bulajić A, Vučurović A, Ristić D, Jović J, Krstić B (2011a) First report of Tomato spotted wilt virus on Gerbera hybrida in Serbia. Plant Dis 95:226. https://doi.org/10.1094/PDIS-10-10-0704
Stanković I, Bulajić A, Vučurović A, Ristić D, Milojević K, Berenji J, Krstić B (2011b) Status of tobacco viruses in Serbia and molecular characterization of Tomato spotted wilt virus isolates. Acta Virol 55:337–347. https://doi.org/10.4149/av_2011_04_337
Stanković I, Bulajić A, Vučurović A, Ristić D, Milojević K, Nikolić D, Krstić B (2012) First report of Tomato spotted wilt virus infecting onion and garlic in Serbia. Plant Dis 96:918. https://doi.org/10.1094/PDIS-02-12-0157-PDN
Stanković I, Bulajić A, Vučurović A, Ristić D, Milojević K, Nikolić D, Krstić B (2013) First report of Tomato spotted wilt virus on chrysanthemum in Serbia. Plant Dis 97:150. https://doi.org/10.1094/PDIS-08-12-0778-PDN
Tentchev D, Verdin E, Marchal C, Jacquet M, Aguilar JM, Moury B (2011) Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes. J Gen Virol 92:961–973. https://doi.org/10.1099/vir.0.029082-0
Thomas-Carrol ML, Jones RAC (2003) Selection, biological properties and fitness of resistance-breaking strains of tomato spotted wilt virus in pepper. Ann Appl Biol 142:235–243. https://doi.org/10.1111/j.1744-7348.2003.tb00246.x
Thompson GJ, Van Zijl JJB (1996) Control of Tomato spotted wilt virus in tomatoes in South Africa. Acta Hort 431:379–384
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position–specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Tsompana M, Moyer JW (2008) Tospoviruses. In: Mahy BWJ, Regenmortel MHV (eds) Encyclopedia of virology, 3rd edn. Elsevier Ltd, Oxford, pp 157–162
Tsompana M, Abad J, Purugganan M, Moyer JW (2005) The molecular population genetics of the Tomato spotted wilt virus (TSWV) genome. Mol Ecol 14:53–66. https://doi.org/10.1111/j.1365-294X.2004.02392.x
Turina M, Kormelink R, Resende RO (2016) Resistance to Tospoviruses in vegetable crops: epidemiological and molecular aspects. Annu Rev Phytopathol 54:347–371. https://doi.org/10.1146/annurev-phyto-080615-095843
Vučurović A, Bulajić A, Stanković I, Ristić D, Berenji J, Jović J, Krstić B (2012) Non-persistently aphid-borne viruses infecting pumpkin and squash in Serbia and partial characterization of Zucchini yellow mosaic virus isolates. Eur J Plant Pathol 133:935–947. https://doi.org/10.1007/s10658-012-9964-x
Whitfield AE, Ullman DE, German TL (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489. https://doi.org/10.1146/annurev.phyto.43.040204.140017
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This research was supported by grant 451–03-9/2021–14/200116 of the Ministry of Education, Science, and Technological Development, Republic of Serbia.
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Petrović, B., Vučurović, A., Zečević, K. et al. Resistance-breaking tomato spotted wilt orthotospovirus isolates on resistant tomato in Serbia. J Plant Dis Prot 128, 1327–1339 (2021). https://doi.org/10.1007/s41348-021-00493-4
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DOI: https://doi.org/10.1007/s41348-021-00493-4