Abstract
In recent years, symptoms of vein yellowing and leaf roll in pepper crops associated with the presence of poleroviruses (genus Polerovirus, family Luteoviridae) have been emerging in many countries worldwide. Spain was the first country in Europe where the yellowing disease of pepper was observed. In this work, a polerovirus isolate from Spain that infects pepper and has been shown to be transmitted by the aphid Aphis gossyppii (Spain-Almería 2-2013) was sequenced and compared with isolates from Japan, Israel, China and Australia. The genome (6125 nt in length, GenBank accession number KY523072) of the isolate from Spain has the typical organization of poleroviruses and contains seven open reading frames (ORF0 to ORF5 and ORF3a), putatively encoding proteins P0 to P5 and P3a. A comparison of the sequence from Spain with the four complete sequences available for poleroviruses infecting pepper showed a closer relationship to the isolate from Israel and supports the existence of a complex of at least five polerovirus species. Given that the symptoms caused by all pepper poleroviruses described to date are similar, if not identical, we propose to name them “pepper vein yellows virus 1” to “pepper vein yellows virus 5” (PeVYV-1 to PeVYV-5), with PeVYV-5 corresponding to the polerovirus from Spain described in this work. Our results and those published over the last few years have shown that the emergent poleroviruses threatening pepper crops around the world are highly complex due to recombination events.




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References
Ibiza VP, Blanca J, Cañizares J, Nuez F (2012) Taxonomy and genetic diversity of domesticated Capsicum species in the Andean region. Genet Resour Crop Ev 59:1077–1088
Gniffke PA, Shieh SC, Lin SW, Sheu ZM, Chen JR, Ho FI et al (2013) Pepper research and breeding at AVRDC—the world vegetable center. In: XV EUCARPIA meeting on genetics and breeding of capsicum and eggplant; Sep 2–4; Turin, Italy. pp 305–311
Moury B, Verdin E (2012) Viruses of pepper crops in the Mediterranean basin: a remarkable stasis. Adv Virus Res 84:127–162
Kenyon L, Kumar S, Tsai WS, Hughes JDA (2014) Virus diseases of peppers (Capsicum spp.) and their control. Adv Virus Res 90:297–354
Yonaha T, Toyosato T, Kawano S, Osaki T (1995) Pepper vein yellows virus, a novel luteovirus from bell pepper plants in Japan. Ann Phytopathol Soc Jpn 61:178–184
Antignus Y, Lachman O, Pearlsman M, Ucko O (2001) A new pepper yellowing disease of pepper caused by an unidentified luteovirus. Phytoparasitica 29:255
Dombrovsky A, Glanz E, Pearlsman M, Lachman O, Antignus Y (2010) Characterization of Pepper yellow leaf curl virus, a tentative new Polerovirus species causing a yellowing disease of pepper. Phytoparasitica 38:477–486
Domier LL (2012) Family Luteoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 1045–1053
International Committee on Taxonomy of Viruses (ICTV). Virus Taxonomy: 2016 Release. http://www.ictvonline.org/virustaxonomy.asp. Accessed 15 Nov 2017
Brault V, Herrbach E, Rodriguez-Medina C (2011) Luteoviruses. eLS. Wiley, Chichester
Fereres A, Raccah B (2015) Insect transmission of plant viruses. eLS. Wiley, Chichester
Smirnova E, Firth AE, Miller WA, Scheidecker D, Brault V, Reinbold C, Rakotondrafara AM, Chung BYW, Ziegler-Graff V (2015) Discovery of a small non-AUG-initiated ORF in poleroviruses and luteoviruses that is required for long-distance movement. PLoS Pathog 11:e1004868
Murakami R, Nakashima N, Hinomoto N, Kawano S, Toyosato T (2011) The genome sequence of pepper vein yellows virus (family Luteoviridae, genus Polerovirus). Arch Virol 156:921–923
Dombrovsky A, Glanz E, Lachman O, Sela N, Doron-Faigenboim A, Antignus Y (2013) The complete genomic sequence of Pepper yellow leaf curl virus (PYLCV) and its implications for our understanding of evolution dynamics in the genus Polerovirus. PLoS One 8:e70722
Liu M, Liu X, Li X, Zhang D, Dai L, Tang Q (2016) Complete genome sequence of a Chinese isolate of pepper vein yellows virus and evolutionary analysis based on the CP, MP and RdRp coding regions. Arch Virol 161:677–683
Maina S, Edwards OR, Jones RAC (2016) First complete genome sequence of Pepper vein yellows virus from Australia. Genome Announc 4:e00450-16
Buzkan N, Arpaci BB, Simon V, Fakhfakh H, Moury B (2013) High prevalence of poleroviruses in field-grown pepper in Turkey and Tunisia. Arch Virol 158:881–885
Villanueva F, Castillo P, Font MI, Alfaro-Fernández A, Moriones E, Navas-Castillo J (2013) First report of Pepper vein yellows virus infecting sweet pepper in Spain. Plant Dis 97:1261
Knierim D, Tsai WS, Kenyon L (2013) Analysis of sequence from field samples reveals the presence of the recently described pepper vein yellows virus (genus Polerovirus) in six additional countries. Arch Virol 158:1337–1341
Alfaro-Fernández A, ElShafie EE, Ali MA, El Bashir OOA, Córdoba-Sellés MC, Font San Ambrosio MI (2014) First report of Pepper vein yellows virus infecting hot pepper in Sudan. Plant Dis 98:1446
Alabi OJ, Al Rwahnih M, Jifon JL, Gregg L, Crosby KM, Mirkov TE (2015) First report of Pepper vein yellows virus infecting pepper (Capsicum spp.) in the United States. Plant Dis 99:1656
Bolou Bi BA, Moury B, Abo K, Kakou D Jr, Girardot G, Kouassi N’dri P et al (2015) First report of Pepper vein yellows virus in field grown pepper in Ivory Coast. J Plant Pathol 97:S67–S77
Zhang SB, Zhao ZB, Zhang DY, Liu Y, Zhang SB, Zhang DY et al (2015) First report of Pepper vein yellows virus infecting red pepper in mainland China. Plant Dis 99:1190
Tan WP, Dong YZ, Sun XH, Liang YC, Liu HX, Zhu XP (2015) The first identification of Pepper vein yellows virus in Shandong Province, China. Plant Dis 99:1288
Tomassoli L, Manglli A, Ahmad A, Tiberini A, Barba M (2016) First report of Pepper vein yellows virus infecting chilli pepper (Capsicum spp.) in Italy. New Dis Rep 33:22
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Muhire BM, Varsani A, Martin DP (2014) SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Fourment M, Gibbs AJ, Gibbs MJ (2008) SWeBLAST: a sliding window web-based BLAST tool for recombinant analysis. J Virol Methods 152:98–101
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:1–5
Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarini SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length Human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India with evidence of intersubtype recombination. J Virol 73:152–160
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267
Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681
Acknowledgements
We are thankful to Paloma Castillo (Laboratory of Plant Production and Health, Regional Government of Andalusia, Almería, Spain) for assistance with field sample collection after consent obtained from farmers, María Dolores Alcázar Alba with identification of aphids, and Francisco Villanueva and Remedios Tovar with aphid transmission and plant growing.
Funding
This work was supported in part by grant P08-AGR-04045 from Consejería de Economía, Innovación y Ciencia, Junta de Andalucía, Spain, co-funded by the European Regional Development Fund and the European Social Fund (ESF). EFO is recipient of a “Juan de la Cierva-Incorporación” contract from the Ministerio de Economía y Competitividad (MINECO), Spain. ENH is the recipient of a predoctoral contract from the MINECO (co-funded by ESF). CGF was the recipient of a sandwich PhD fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Science Without Borders program), Brazil.
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Fiallo-Olivé, E., Navas-Hermosilla, E., Ferro, C.G. et al. Evidence for a complex of emergent poleroviruses affecting pepper worldwide. Arch Virol 163, 1171–1178 (2018). https://doi.org/10.1007/s00705-018-3733-x
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DOI: https://doi.org/10.1007/s00705-018-3733-x