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Biological and molecular characterization of Tomato spotted wilt orthotospovirus isolates from pepper cultivars with the resistance gene Tsw from Turkey

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Abstract

Tomato spotted wilt orthotospovirus (TSWV) is one of the most widespread and damaging pepper viruses worldwide. Until recently, disease control has been achieved by breeding pepper cultivars with the resistance gene Tsw. However, the breakdown of Tsw-resistance gene has been increasingly reported from many locations where resistant cultivars have been grown. This has been caused by the emergence of resistance-breaking isolates because of the high evolutionary and adaptative capacity of TSWV. The resurgence of RB TSWV-strains causing heavy production losses in pepper (Capsicum annuum) plants in Turkey has directed the attention to the factors contributing to the outbreak of these serious epidemics. In this paper, we report the first detailed molecular and biological characterization of TSWV-isolates in the field and greenhouse-grown pepper plants. Biological clones from TSWV field samples segregated into three different types of symptoms on pepper plants carrying the Tsw-resistance gene; (i) only local lesions as a result of hypersensitive reaction, (ii) chlorotic rings, chlorosis, vein clearing, downward leaf curling, and stunting, (iii) severe systemic necrosis and wilting leading to the death of resistant plants. The phylogenetic analysis of the NSs gene has shown that the isolates were clustered regardless of the phenotype RB or non-resistance breaking (NRB). Our study has also supported the hypothesis that developing and expanding the RB isolates has occurred locally. The phylogenetic analyses on TSWV-pepper isolates have revealed the fact for the presence of reassortment in TSWV population which might be caused by a mixed infection of TSWV variants.

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References

  • Adkins S (2000) Tomato spotted wilt virus-positive steps towards negative success. Mol Plant Pathol 1(3):151–157

    Article  CAS  Google Scholar 

  • Almási A, Nemes K, Salánki K (2020) Increasing diversity of resistance breaking pepper strains of Tomato spotted wilt virus in the Mediterranean region. Phytopathol Mediterr 59(2):385–391. https://doi.org/10.14601/Phyto-11346

    Article  Google Scholar 

  • Arlı-Sökmen M, Mennan H, Sevik MA, Ecevit O (2005) Occurrence of viruses in field-grown pepper crops and some of their reservoir weed hosts in Samsun, Turkey. Phytoparastica 33(4):347–358. https://doi.org/10.1007/BF02981301

    Article  Google Scholar 

  • Azeri T (1981) Preliminary report of tomato spotted wilt virus and its epidemy on tobacco in the Çanakkale region of Turkey. J Turk Phytopathol 10(2–3):79–87

    Google Scholar 

  • Black LL, Hobbs HA, Gatti JM Jr (1991) Tomato spotted wilt virus resistance in Capsicum chinense PI 152225 and 159236. Plant Dis 75:863. https://doi.org/10.1094/PD-75-0863A

    Article  Google Scholar 

  • Black LL, Hobbs HA, Kammerlohr DS (1996) Resistance of Capsicum chinense lines to tomato spotted wilt virus isolates from Louisiana, USA, and inheritance of resistance. Acta Hortic 431:393–401. https://doi.org/10.17660/ActaHortic.1996.431.34

    Article  Google Scholar 

  • Boiteux LS (1995) Allelic relationships between genes for resistance to tomato spotted wilt tospovirus in Capsicum chinense. Theor Appl Genet 90:146–149

    Article  CAS  Google Scholar 

  • Boiteux LS, Nagata T (1993) Susceptibility of Capsicum chinense PI 159236 to tomato spotted wilt virus isolates in Brazil. Plant Dis 77:210. https://doi.org/10.1094/PD-77-0210F

    Article  Google Scholar 

  • Çelik İ, Özalp R, Çelik N, Polat İ, Sülü G (2018) Improvement of long type pepper lines resistant to tomato spotted wilt virus (TSWV). Derim 35(1):27–36. https://doi.org/10.16882/derim.2018.325765

    Article  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162(1):156–159. https://doi.org/10.1006/abio.1987.9999 (PMID: 2440339)

    Article  CAS  Google Scholar 

  • Chung BN, Choi HS, Yang EY, Cho JD, Cho IS, Choi GS, Choi SK (2012) Tomato spotted wilt virus isolates giving different infection in Commercial Capsicum annuum cultivars. Plant Pathol J 28(1):87–92. https://doi.org/10.5423/PPJ.NT.09.2011.0169

    Article  CAS  Google Scholar 

  • Clark MF, Adams AN (1977) Characteristic of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J Gen Virol 34:475–483. https://doi.org/10.1099/0022-1317-34-3-475

    Article  CAS  Google Scholar 

  • Cortez I, Saaijer J, Wongjkaew KS, Pereira AM, Goldbach R, Peters D, Kormelink R (2001) Identification and characterization of a novel tospovirus species using a new RT-PCR approach. Adv Virol 146:265–278. https://doi.org/10.1007/s007050170174

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • de Ronde D, Butterbach P, Lohuis D, Heild 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. Adv Virol 160(8):2117–2123. https://doi.org/10.1007/s00705-015-2453-8

    Article  CAS  Google Scholar 

  • Deligöz I, Sökmen MA, Sarı 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

    Article  Google Scholar 

  • Fidan H, Koç G, Topçu T (2016) Infection and molecular characterization of tomato spotted wilt virus (TSWV) on Anthurium sp. Alatarım 15(2):28–36

    Google Scholar 

  • Francki RIB, Hatta T (1981) Tomato spotted wilt virus. In: Kurstak E (ed) Handbook of Plant Virus Infections and Comparative Diagnosis. Elsevier/North- Holland Biomedical Press, Amsterdam, pp 491–512

    Google Scholar 

  • Garnsey SM, Randles JW (1987) Biological interactions and agricultural implications of viroids. In: Semancik JS (ed) Viroids and viroid-like pathogens. CRC Press, Boca Raton, FL, pp 127–160

    Google Scholar 

  • Goldbach R, Peters D (1996) Molecular and biological aspects of tospoviruses. In: Elliott RM (ed) The Bunyaviridae. Plenum Press, New York

    Google Scholar 

  • Griep RA, Prins M, van Twisk C, Keller HJHG, Kerschbaumer RJ, Kormelink R, Golbach RW, Schots A (2000) Application of Phage display in selecting tomato spotted wilt virus –Specific single -Chain antibodies (scFvs) for sensetive diagnosis in ELISA. Phytopathology 90:183–190

    Article  CAS  Google Scholar 

  • Güneş N, Gümüş M (2019) Detection and characterization of tomato spotted wilt virus and cucumber mosaic virus on pepper growing areas in Antalya. J Agric Sci 25:259–271

    Google Scholar 

  • Hoang NH, Yang HB, Kang BC (2013) Identification and inheritance of a new source of resistance against tomato spotted wilt virus (TSWV) in Capsicum. Sci Hortic 161:8–14

    Article  CAS  Google Scholar 

  • Hobbs HA, Black LL, Johnson RR, Valverde RA (1994) Differences in reactions among tomato spotted wilt virus isolates to three resistant Capsicum chinense lines. Plant Dis 78:1220 (Abstr.)

    Article  Google Scholar 

  • Kamberoğlu MA, Calışkan AF, Alan B (2009) First Report of tomato spotted wilt virus on eggplant in Turkey. J Plant Pathol 91(1):231–231

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  • Lian S, Lee JS, Cho WK, Yu J, Kim MK, Choi HS, Kim KH (2013) Phylogenetic and recombination analysis of tomato spotted wilt virus. PLoS ONE 8(5):e63380. https://doi.org/10.1371/journal.pone.0063380

    Article  CAS  Google Scholar 

  • Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Inger-soll R, Sheppard HW, Ray SC (1999) Full-length human immuno deficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of inter subtype recombination. J Virol 73:152–160. https://doi.org/10.1128/jvi.73.1.152-160.1999

    Article  CAS  Google Scholar 

  • Macedo MA, Rojas MR, Gilbertson RL (2019) First report of a resistance-breaking strain of Tomato spotted wilt orthotospovirus infecting sweet pepper with the Tsw resistance gene in California, USA. Plant Dis 103(5):1048. https://doi.org/10.1094/PDIS-07-18-1239-PDN

    Article  Google Scholar 

  • Mandal B, Pappu HR, Csinos AS, Culbreath AK (2006) Response of peanut, pepper, tobacco, and tomato cultivars to two biologically distinct isolates of tomato spotted wilt virus. Plant Dis 90:1150–1155. https://doi.org/10.1094/PD-90-1150

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Margaria P, Ciuffo M, Turina M (2004) Resistance breaking strain of tomato spotted wilt virus (Tospovirus; Bunyaviridae) on resistant pepper cultivars in Almeria, Spain. Plant Pathol 53:795–795. https://doi.org/10.1111/j.1365-3059.2004.01082.x

    Article  Google Scholar 

  • Margaria P, Miozzi L, Ciuffo M, Pappu H, Turina M (2014) The first complete genome sequences of two distinct European tomato spotted wilt virus isolates. Arch Virol 160:591–595. https://doi.org/10.1007/s00705-014-2256-3

    Article  CAS  Google Scholar 

  • Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003. https://doi.org/10.1093/ve/vev003

    Article  Google Scholar 

  • McPherson RM, Jones DC, Pappu HR, Moore JM (2003) Reducing the risks of spotted wilt virus in tobacco with selected Thrips (Thysanoptera: Thripidae) control practices. J Agric Urban Entomol 20(1):11–23

    Google Scholar 

  • Moury B, Palloix A, Gebre-Selassie K, Marchoux G (1997) Hypersensitive resistance to tomato spotted wilt virus in three Capsicum chinense accessions is controlled by a single gene and is overcome by virulent strains. Euphytica 94:45–52

    Article  Google Scholar 

  • Moury B, Verdin E (2012) Viruses of pepper crops in the Mediterranean basin: a remarkable stasis. Adv Virus Res 84:127–162

    Article  Google Scholar 

  • Naidu RA, Sherwood JL, Deom CM (2008) Characterization of a vector-non-transmissible isolate of tomato spotted wilt virus. Plant Pathol 57:190–200

    CAS  Google Scholar 

  • Pappu HR, Jones RAC, Jain RK (2009) Global status of tospovirus epidemics in diverse cropping systems: Successes achieved and challenges ahead. Virus Res 141:219–236. https://doi.org/10.1016/j.virusres.2009.01.009

    Article  CAS  Google Scholar 

  • Pappu HR, Whitfield AE, de Oliveria AS (2020) Tomato spotted wilt virus (Tospoviridae). Elseveir. https://doi.org/10.1016/B978-0-12-809633-8.21329-0

    Book  Google Scholar 

  • Parrella G, Gognalons P, Gebre-Selassie K, Vovlas C, Marchoux G (2003) An update of the host range of tomato spotted wilt virus. J Plant Pathol 85:227–264

    Google Scholar 

  • Persley DM, Thomas JE, Sharman M (2006) Tospoviruses: an Australian perspective. Australas Plant Pathol 35:161–180. https://doi.org/10.1071/AP06015

    Article  Google Scholar 

  • Riley DG, Joseph SV, Srinivasan R, Diffie S (2011) Thrips vectors of tospoviruses. J Integr Pest Manag 2:1–10. https://doi.org/10.1603/IPM10020

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Scholthof KB, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Hemenway C, Foster GD (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12(9):938–954. https://doi.org/10.1111/j.1364-3703.2011.00752.x

    Article  CAS  Google Scholar 

  • Sertkaya G (2015) Investigation of some viruses in lettuce and spinach fields in Hatay province of Turkey. Mustafa Kemal Univ J Agric Sci 20(1):7–12

    Google Scholar 

  • Sharman M, Persley DM (2006) Field isolates of tomato spotted wilt virus overcoming resistance in capsicum in Australia. Australas Plant Pathol 35:123–128. https://doi.org/10.1071/AP06014

    Article  Google Scholar 

  • Şimşek D, Pınar H, Mutlu N (2015) Development of new bell pepper (Capsicum annum L.) lines and cultivars resistance to tospovirus and tobamovirus using molecular breeding methods. Alatarım 14(1):1–8

    Google Scholar 

  • Sin SH, McNulty BC, Kennedy GG, Moyer JW (2005) Viral genetic determinants for thrips transmission of tomato spotted wilt virus. Proc Natl Acad Sci USA 102:5168–5173

    Article  CAS  Google Scholar 

  • Soler S, Diez MJ, Nuez F (1998) Effect of temperature regime and growth stage interaction on pattern of virus presence in TSWV-resistant accessions of Capsicum chinense. Plant Dis 82:1199–1204. https://doi.org/10.1094/PDIS.1998.82.11.1199

    Article  Google Scholar 

  • Takeda A, Sugiyama K, Nagano H, Mori M, Kaido M, Mise K, Tsuda S, Okuno T (2002) Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett 532:75–79. https://doi.org/10.1016/s0014-5793(02)03632-3

    Article  CAS  Google Scholar 

  • Tekinel N (1973) Investigations on the dissemination and rates of tomato virus disease Adana, Antalya, Hatay, and Içel provinces. Plant Prot Bull 13(3):107–141

    Google Scholar 

  • Tekinel N, Dolar MS, Sağsöz S, Salcan Y (1969) Research on viruses of some economically important vegetables in the Mersin region. Plant Prot Bull 9:37–49

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Thekke-Veetil T, Polashock JJ, Marn MV, Plesko IM, Schilder AC, Keller KE, Martin RR, Tzanetakis IE (2015) Population structure of blueberry mosaic associated virus: Evidence of reassortment in geographically distinct isolates. Virus Res 2(201):79–84. https://doi.org/10.1016/j.virusres.2015.02.022

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yurtmen M, Güldür ME, Yılmaz MA (1998) Tomato spotted wilt virus on pepper in Içel province of Turkey. Ninth Conference of the I.S.H.S Vegetable Virus Working Group, Recent Advance in Vegetable Virus Research, Torino, Italy, pp 91–92, 22–27 August 1998

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Funding

This work was supported by the Research Fund of Kahramanmaraş Sütçü Imam University (Project No: 2019/3–18 M). We are grateful to Dr. Bekir Bülent Arpacı for valuable suggestions.

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  1. Agriculture Faculty Plant Protection Department, Kahramanmaras Sütçü Imam University, Kahramanmaras, 46050, Turkey

    Selin Ceren Balsak & Nihal Buzkan

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  1. Selin Ceren Balsak
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Correspondence to Selin Ceren Balsak.

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Balsak, S.C., Buzkan, N. Biological and molecular characterization of Tomato spotted wilt orthotospovirus isolates from pepper cultivars with the resistance gene Tsw from Turkey. Australasian Plant Pathol. 51, 543–551 (2022). https://doi.org/10.1007/s13313-022-00890-9

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