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East Asian Passiflora distortion virus: a novel potyvirus species causing deformation of passionfruits in Japan

  • Viral and Viroid Diseases
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Abstract

Viruses assumed to belong to a new Potyvirus were detected in passionfruit plants with foliar mosaic, leaf curl and fruit malformation that were collected from Akita City, Akita Prefecture in 2013, Nago City, Okinawa Prefecture in 2014, and Satsuma Town and Yoron Island, Kagoshima Prefecture in 2015. The isolates of this virus species were not detected by ELISA and RT-PCR targeting East Asian Passiflora virus (EAPV)-AO (Amami Oshima strain), which induces woodiness disease of passionfruit in Japan. The isolates were designated PV-AK (Akita), PV-OK (Okinawa), PV-YO (Yoron), and PV-SA (Satsuma). In a host-range test of 13 cultivars of French bean, four were systemically infected with the PV isolates and two with EAPV-AO. Cowpea cv. Kurodane sanjaku was systemically infected with PV isolates and induced mosaic symptoms on non-inoculated leaves distant from the inoculated leaves but was immune to EAPV-AO. The complete genomic sequences of the PV isolates consisted of 9973 nucleotides (nt) excluding the poly(A) tail, and encoded 3217 amino acids of polyprotein, flanked by 129–130 nt of the 5′-noncoding region and 193 nt of the 3′-noncoding region. Whole-genome nucleotide and amino acid sequences indicated that they belong to identical species. The potyvirus with the highest whole-genome nucleotide identity to the PV isolates is watermelon mosaic virus, which shares 68.1% identity, versus 65.3% for EAPV-AO. On the basis of ICTV-naming regulations, these PV isolates belong to a new species in the Potyvirus genus, but are distantly related to EAPV. Here, we propose East Asian Passiflora distortion virus as the new species name.

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References

  • Adams MJ, Antoniw JF, Beaudoin F (2005a) Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 6:471–487

    CAS  PubMed  Google Scholar 

  • Adams MJ, Antoniw JF, Fauquet CM (2005b) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150:459–479

    CAS  PubMed  Google Scholar 

  • Aguilar E, Allende L, del Toro FJ, Chung BN, Canto T, Tenllado F (2015) Effects of elevated CO2 and temperature on pathogenicity determinants and virulence of Potato virus X/Potyvirus-associated synergism. Mol Plant Microbe Interact 28:1364–1373

    CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  Google Scholar 

  • Ateka E, Alicai T, Ndunguru J, Tairo F, Sseruwagi P, Kiarie S, Makori T, Kehoe MA, Boykin LM (2017) Unusual occurrence of a DAG motif in the ipomovirus Cassava brown streak virus and implications for its vector transmission. PLoS One 12:e0187883

    PubMed  PubMed Central  Google Scholar 

  • Atreya PL, López-Moya JJ, Chu M, Atreya CD, Pirone TP (1995) Mutational analysis of the coat protein N-terminal amino acids involved in potyvirus transmission by aphids. J Gen Virol 76:265–270

    CAS  PubMed  Google Scholar 

  • Babu B, Hegde V (2014) Molecular characterization of Dasheen mosaic virus isolates infecting edible aroids in India. Acta Virol 58:34–42

    CAS  PubMed  Google Scholar 

  • Blanc S, López-Moya JJ, Wang R, Garcia-Lampasona S, Thornbury DW, Pirone TP (1997) A specific interaction between coat protein and helper component correlates with aphid transmission of a potyvirus. Virology 231:141–147

    CAS  PubMed  Google Scholar 

  • Blystad DR, van der Vlugt R, Alfaro-Fernández A, Córdoba MDC, Bese G, Hristova D, Pospieszny H, Mehle N, Ravnikar M, Tomassoli L, Varveri C, Nielsen SL (2015) Host range and symptomatology of Pepino mosaic virus strains occurring in Europe. Eur J Plant Pathol 143:43–56

    Google Scholar 

  • Cerqueira-Silva CBM, Faleiro FG, de Jesus ON, dos Santos ESL, de Souza AP (2016) The genetic diversity, conservation, and use of passion fruit (Passiflora spp.). In: Ahuja MR, Jain SM (eds) Genetic diversity and erosion in plants, sustainable development and biodiversity, vol 8. Springer, Cham, pp 215–231

    Google Scholar 

  • Chiemsombat P, Prammanee S, Pipattanawong N (2014) Occurrence of Telosma mosaic virus causing passion fruit severe mosaic disease in Thailand and immunostrip test for rapid virus detection. Crop Protect 63:41–47

    Google Scholar 

  • Ciuffo M, Mammella M, Vallino M, Caciagli P, Turina M (2016) Molecular identification and biological characterization of a new potyvirus in lettuce. Arch Virol 161:2549–2554

    CAS  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    CAS  Google Scholar 

  • Domier LL, Shaw JG, Rhoads RE (1987) Potyviral proteins share amino acid sequence homology with picorna-, como-, and caulimoviral proteins. Virology 158:20–27

    CAS  PubMed  Google Scholar 

  • Domier LL, Latorre IJ, Steinlage TA, McCoppin N, Hartman GL (2003) Variability and transmission by Aphis glycines of North American and Asian soybean mosaic virus isolates. Arch Virol 148:1925–1941

    CAS  PubMed  Google Scholar 

  • Dougherty WG, Parks TD, Cary SM, Bazan JF, Fletterick RJ (1989) Characterization of the catalytic residues of the tobacco etch virus 49-kDa proteinase. Virology 172:302–310

    CAS  PubMed  Google Scholar 

  • Fernández A, Guo HS, Sáenz P, Simón-Buela L, Gómez de Cedrón M, Garcia JA (1997) The motif V of plum pox potyvirus CI RNA helicase is involved in NTP hydrolysis and is essential for virus RNA replication. Nucleic Acids Res 25:4474–4480

    PubMed  PubMed Central  Google Scholar 

  • Fukumoto T, Nakamura M, Rikitake M, Iwai H (2012) Molecular characterization and specific detection of two genetically distinguishable strains of East Asian Passiflora virus (EAPV) and their distribution in southern Japan. Virus Genes 44:141–148

    CAS  PubMed  Google Scholar 

  • Gal-On A (2000) A point mutation in the FRNK motif of the potyvirus helper component-protease gene alters symptom expression in cucurbits and elicits protection against the severe homologous virus. Phytopathology 90:467–473

    CAS  PubMed  Google Scholar 

  • Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant–pathogen interactions. Mol Plant Microbe Interact 21:1015–1026

    CAS  PubMed  Google Scholar 

  • Hamilton RI, Edwardson JR, Francki RIB, Hsu HT, Hull R, Koenig R, Milne RG (1981) Guidelines for the identification and characterization of plant viruses. J Gen Virol 54:223–241

    CAS  Google Scholar 

  • Huet H, Gal-On A, Meir E, Lecoq H, Raccah B (1994) Mutations in the helper component protease gene of zucchini yellow mosaic virus affect its ability to mediate aphid transmissibility. J Gen Virol 75:1407–1414

    CAS  PubMed  Google Scholar 

  • Iwai H (2017) Studies on the diagnosis and genomic analysis of plant viral diseases in southern Japan. J Gen Plant Pathol 83:414–418

    Google Scholar 

  • Iwai H, Ohmori T, Kurokawa Y, Muta T, Arai K (1996) New record of passionfruit woodiness virus in Japan. Ann Phytopathol Soc Jpn 62:459–465

    Google Scholar 

  • Iwai H, Yamashita Y, Nishi N, Nakamura M (2006) The potyvirus associated with the dappled fruit of Passiflora edulis in Kagoshima Prefecture, Japan is the third strain of the proposed new species East Asian Passiflora virus (EAPV) phylogenetically distinguished from strains of Passion fruit woodiness virus. Arch Virol 151:811–818

    CAS  PubMed  Google Scholar 

  • Kidanemariam DB, Abraham AD, Sukal AC, Holton TA, Dale JL, James AP, Harding RM (2016) Complete genome sequence of a novel zantedeschia mild mosaic virus isolate: the first report from Australia and from Alocasia sp. Arch Virol 161:1079–1082

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  • Lan P, Li F, Wang M, Li R (2015) Complete genome sequence of a divergent strain of Japanese yam mosaic virus from China. Arch Virol 160:573–576

    CAS  PubMed  Google Scholar 

  • Langeveld SA, Dore JM, Memelink J, Derks AF, van der Vlugt CI, Asjes CJ, Bol JF (1991) Identification of potyviruses using the polymerase chain reaction with degenerate primers. J Gen Virol 72:1531–1541

    CAS  PubMed  Google Scholar 

  • Li MJ, Kim JK, Seo EY, Hong SM, Hwang EI, Moon JK, Domier LL, Hammond J, Youn YN, Lim HS (2014) Sequence variability in the HC-Pro coding regions of Korean soybean mosaic virus isolates is associated with differences in RNA silencing suppression. Arch Virol 159:1373–1383

    CAS  PubMed  Google Scholar 

  • Malpica JM, Fraile A, Moreno I, Obies CI, Drake JW, Garcia-Arenal F (2002) The rate and character of spontaneous mutation in an RNA virus. Genetics 162:1505–1511

    CAS  PubMed  PubMed Central  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

    PubMed  PubMed Central  Google Scholar 

  • Monjero K, Mbogo E, Irungu J, Miano D (2015) Establishment of Nicotiana benthamiana in the green house. Schol J Agric Sci 5:59–62

    Google Scholar 

  • Riechmann JL, Lain S, Garcia JA (1992) Highlights and prospects of potyvirus molecular biology. J Gen Virol 73:1–16

    CAS  PubMed  Google Scholar 

  • Shiboleth YM, Harosnky E, Leibman D, Arazi T, Wassenegger M, Whitham SA, Gaba V, Gal-On A (2007) The conserved FRNK box in HC-Pro, a plant viral suppressor of gene silencing, is required for small RNA binding and mediates symptom development. J Virol 81:13135–13148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shukla DD, Ward CW (1989) Structure of potyvirus coat proteins and its application in the taxonomy of the Potyvirus group. Adv Virus Res 36:273–314

    CAS  PubMed  Google Scholar 

  • Shukla DD, Frcnkel MJ, Ward CW (1991) Structure and function of the potyvirus genome with special reference to the coat protein coding region. Can J Plant Pathol 13:178–191

    CAS  Google Scholar 

  • Su X, Fu S, Qian Y, Zhang L, Xu Y, Zhou X (2016) Discovery and small RNA profile of Pecan mosaic-associated virus, a novel potyvirus of pecan trees. Sci Rep 6:26741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Urcuqui-Inchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74:157–175

    CAS  PubMed  Google Scholar 

  • Van Dijk P, van der Meer FA, Piron PGM (1987) Accessions of Australian Nicotiana species suitable as indicator hosts in the diagnosis of plant virus diseases. Neth J Plant Pathol 93:73–85

    Google Scholar 

  • Wang HY, Liu JL, Gao R, Chen J, Shao YH, Li XD (2009) Complete genomic sequence analyses of Turnip mosaic virus basal-BR isolates from China. Virus Genes 38:421–428

    CAS  PubMed  Google Scholar 

  • Watanabe M, Noda C, Maoka T, Usugi T, Natsuaki KT (1997) Occurrence of Passiflora latent virus in Japan (abstract in Japanese). Jpn J Phytopathol 63:194

    Google Scholar 

  • Wylie SJ, Jones MG (2011) The complete genome sequence of a Passion fruit woodiness virus isolate from Australia determined using deep sequencing, and its relationship to other potyviruses. Arch Virol 156:479–482

    CAS  PubMed  Google Scholar 

  • Wylie SJ, Kueh J, Welsh B, Smith LJ, Jones MGK, Jones RAC (2002) A non-aphid-transmissible isolate of bean yellow mosaic potyvirus has an altered NAG motif in its coat protein. Arch Virol 147:1813–1820

    CAS  PubMed  Google Scholar 

  • Wylie SJ, Adams M, Chalam C, Kreuze J, López-Moya JJ, Ohshima K, Praveen S, Rabenstein F, Stenger D, Wang A, Zerbini FM, ICTV Report Consortium (2017) ICTV virus taxonomy profile: Potyviridae. J Gen Virol 98:352–354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yonaha T, Tamori M, Yamanoha S, Nakasone T (1979) Studies on passionfruit virus diseases in Okinawa: 1. Cucumber mosaic virus isolated from diseased Passiflora edulis and Passiflora foetida plants (in Japanese with English summary). Sci Bull Coll Agric Univ Ryukyus 26:29–38

    Google Scholar 

  • Yonaha T, Hiraiwa T, Ooisi T (1993) Broad bean wilt virus isolated from passionfruit (Abstract in Japanese). Jpn J Phytopathol 59:335

    Google Scholar 

  • Zheng L, Gibbs MJ, Rodoni BC (2008) Quantitative PCR measurements of the effects of introducing inosines into primers provides guidelines for improved degenerate primer design. J Virol Methods 153:97–103

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge Dr. E. W. Kitajima, University of Sao Paulo, Brazil, and the Genetic Resources Division, Central Agricultural Research Department (CARD), Hokkaido Research Organization (HRO), for providing the French bean seeds. We also acknowledge Dr. A. Shimada of the fruit horticulture laboratory at the Faculty of Agriculture, Kagoshima University, for useful information on the occurrence of viral diseases in passionfruit producing areas. This work was supported by a JSPS KAKENHI Grant number 16K07620 and by World Bank Funds regulated by the Indonesian Agency of Agriculture Research and Development (IAARD).

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Correspondence to Hisashi Iwai.

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Riska, Sato, Y., Inudo, K. et al. East Asian Passiflora distortion virus: a novel potyvirus species causing deformation of passionfruits in Japan. J Gen Plant Pathol 85, 221–231 (2019). https://doi.org/10.1007/s10327-019-00842-0

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