Abstract
Banana bract mosaic virus (BBrMV) has never been reported in banana plants in Hawaii. In 2010, however, it was detected in a new host, flowering ginger (Alpinia purpurata). In this study, we characterize the A. purpurata isolate and study its spread in flowering ginger in Hawaii. A laboratory study demonstrated that BBrMV could be transmitted from flowering ginger to its natural host, banana, therefore raising a serious concern about the potential risk to the rapidly growing banana industry of Hawaii. To quickly monitor this virus in the field, we developed a robust immunocapture reverse transcription loop-mediated isothermal amplification (IC-RT-LAMP) assay. Deep sequencing of the BBrMV isolate from A. purpurata revealed a single-stranded RNA virus with a genome of 9,713 nt potentially encoding a polyprotein of 3,124 aa, and another predicted protein, PIPO, in the +2 reading-frame shift. Most of the functional motifs in the Hawaiian isolate were conserved among the genomes of isolates from one found in the Philippines and India. However, the A. purpurata isolate had an amino acid deletion in the Pl protein that was most similar to the Philippine isolate. Phylogenetic analysis of an eastern Pacific subpopulation that included A. purpurata was closest in genetic distance to a Southeast Asian subpopulation, suggesting frequent gene flow and supporting the hypothesis that the A. purpurata isolate arrived in Hawaii from Southeast Asia.
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References
Magnaye LV, Espino RRC (1990) NOTE: banana bract mosaic, a new disease of banana, I. Symptomatology. Philipp Agric 73(1):55–59
Kumar PL, Selvarajan R, Iskra-Caruana ML, Chabannes M, Hanna R (2015) Biology, etiology, and control of virus diseases of banana and plantain. Adv Virus Res 91:229–269
Quito-Avila DF, Ibarra MA, Alvarez RA, Ratti MF, Espinoza L, Cevallos-Cevallos JM, Peralta EL (2013) First report of Banana bract mosaic virus in ‘Cavendish’ banana in Ecuador. Plant Dis 97:1003
Wang IC, Sether DM, Melzer MJ, Borth WB, Hu JS (2010) First report of banana bract mosaic virus in flowering ginger in Hawaii. Plant Dis 94:921
Rodoni BC, Ahlawat YS, Varma A, Dale JL, Harding RM (1997) Identification and characterization of banana bract mosaic virus in India. Plant Dis 81:669–672
Thomas JE, Geering ADW, Gambley CF, Kessling AF, White M (1997) Purification, properties and diagnosis of banana bract mosaic potyvirus and its distinction from Abaca mosaic potyvirus. Phytopathology 87:698–705
Ha C, Coombs S, Revil PA, Harding RM, Vu M, Dale JL (2008) Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Arch Virol 153:25–36
Balasubramanian V, Selvarajan R (2012) Complete genome sequence of a banana bract mosaic virus isolate infecting the French plantain cv. Nendran in India. Arch Virol 157:397–400
Wyant PS, Strohmeier S, Schäfer B, Krenz B, Assunção IP, de Andrade Lima GS, Jeske H (2012) Circular DNA genomics (circomics) exemplified for geminiviruses in bean crops and weeds of northeastern Brazil. Virology 427:151–157
Idris A, Al-Saleh M, Piatek MJ, Al-Shahwan I, Ali S, Brown JK (2014) Viral metagenomics: analysis of begomoviruses by illumina high-throughput sequencing. Viruses 12:1219–1236
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
Marais A, Faure C, Couture C, Bergey B, Gentit P, Candresse T (2014) Characterization by deep sequencing of divergent Plum bark necrosis stem pitting virus isolates and development of a broad-spectrum PBNSPaV detection assay. Phytopathology 104:660–666
Al Rwahnih M, Daubert S, Urbez-Torres JR, Cordero F, Rowhani A (2011) Deep sequencing evidence from single grapevine plants reveals a virome dominated by mycoviruses. Arch Virol 156:397–403
Elbeaino T, Giampetruzzi A, De Stradis A, Digiaro M (2014) Deep-sequencing analysis of an apricot tree with vein clearing symptoms reveals the presence of a novel betaflexivirus. Virus Res 181:1–5
Pantaleo V, Saldarelli P, Miozzi L, Giampetruzzi A, Gisel A, Moxon S, Dalmay T, Bisztray G, Burgyan J (2010) Deep sequencing analysis of viral short RNAs from an infected Pinot Noir grapevine. Virology 408:49–56
Yang X, Wang Y, Guo W, Xie Y, Xie Q, Fan L, Zhou X (2011) Characterization of small interfering RNAs derived from the Geminivirus/Betasatellite complex using deep sequencing. PLoS One 6:e16928
Melzer MJ, Sugano JS, Uchida JY, Borth WB, Kawate MK, Hu JS (2013) Molecular characterization of closteroviruses infecting Cordyline fruticosa L. in Hawaii. Front Microbiol. doi:10.3389/fmicb.2013.00039
Marais A, Faure C, Mustafayev E, Barone M, Alioto D, Candresse T (2015) Characterization by deep sequencing of Prunus virus T, a novel Tepovirus infecting Prunus species. Phytopathology 105(1):135–140
Illg RD, Faria RT (1995) Micropropagation of Alpinia purpurata from inflorescence buds. Plant Cell Tissue Organ Cult 40(2):183–185
Paret ML, de Silva AS, Criley RA, Alvarez AM (2008) Ralstonia solanacearum race 4: risk assessment for edible ginger and floricultural ginger industries in Hawaii. Hort Technol 18(1):90–96
Selvarajan R, Jeyabaskaran KJ (2006) Effect of Banana bract mosaic virus (BBrMV) on growth and yield of cultivar Nendran (Plantain, AAB). Indian Phytopathol 59(4):496–500
D’Hont A, Denoeud F, Aury J et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–219
Evans E, Ballen F (2012) Banana Market. Food and Resource Economics Department, UF/IFAS Extension. http://edis.ifas.ufl.edu/fe901
Iskra-Caruana M, Galzi S, Laboureau N (2008) A reliable IC One-step RT-PCR method for the detection of BBrMV to ensure safe exchange of Musa germplasm. J Virol Methods 153:223–231
Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28:e63
Tomita N, Mori Y, Kanda H, Notomi T (2008) Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nat Protoc 3:877–882
Parida M, Posadas G, Inoue S, Hasebe F, Morita K (2004) Real-time reverse transcription loop-mediated isothermal amplification for rapid detection of West Nile virus. J Clin Microbiol 42:257–263
Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858
Hu JS, Gonsalves A, Sether D, Ullman DE (1993) Detection of pineapple closterovirus, a possible cause of mealybug wilt of pineapple. Acta Hortic (ISHS) 334:411–416
Froussard P (1992) A random-PCR method (rPCR) to construct whole cDNA library from low amounts of RNA. Nucleic Acids Res 20:2900
Melzer MJ, Borth WB, Sether DM, Ferreira S, Gonsalves D, Hu JS (2010) Genetic diversity and evidence for recent modular recombination in Hawaiian Citrus tristeza virus. Virus Genes 40:111–118
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580
Hofmann K, Stoffel W (1993) TMbase—a database of membrane spanning proteins segments. Biol Chem Hoppe Seyler 374:166
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406–3415
Urcuqui-Inchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74:157–175
Moury B, Morel C, Johansen E, Jacquemond M (2002) Evidence for diversifying selection in Potato virus Y and in the coat protein of other potyviruses. J Gen Virol 83:2563–2573
Melgarejo TA, Alminaite A, Fribourg C, Spetz C, Valkonen JPT (2004) Strains of Peru tomato virus infecting cocona (Solanum sessiliflorum), tomato and pepper in Peru with reference to genome evolution in genus Potyvirus. Arch Virol 149:2025–2034
Higgins D, Thompson J, Gibson T, 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
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. doi:10.1093/ve/vev003
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014
Balasubramanian V, Selvarajan R (2014) Genetic diversity and recombination analysis in the coat protein gene of Banana bract mosaic virus. Virus Genes 48:509–517
Wei TY, Yang JG, Liao FL, Gao FL, Lu LM, Zhang XT, Li F, Wu ZJ, Lin QY, Xie LH, Lin HX (2009) Genetic diversity and population structure of rice stripe virus in China. J Gen Virol 90:1025–1034
Kadare G, Haenni AL (1997) Virus-encoded RNA helicases. J Virol 71:2583–2590
Murphy JF, Klein PG, Hunt AG, Shaw JG (1996) Replacement of the tyrosine residue that links a potyviral VPg to the viral RNA is lethal. Virology 220:535–538
Siljo A, Bhat AI (2014) Reverse transcription loop-mediated isothermal amplification assay for rapid and sensitive detection of Banana bract mosaic virus in cardamom (Elettaria cardamomum). Eur J Plant Pathol 138:209–214
Coutts RHA, Livieratos IC (2003) A rapid method for sequencing the 5’- and 3’-termini of double-stranded RNA viral templates using RLM-RACE. J Phytopathol 151:525–527
Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts—amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002
Adams MJ, Antoniw JF, Beaudoin F (2005) Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 6:471–487
Chung BY, Miller WA, Atkins JF, Firth AE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci USA 105(15):5897–5902
Glasa M, Svoboda J, Nováková S (2007) Analysis of the molecular and biological variability of zucchini yellow mosaic virus isolates from Slovakia and Czech Republic. Virus Genes 35:415–421
Yan Q (2008) Bioinformatics databases and tools in virology research: an overview. In Silico Biol 8:71–85
Letunic I, Doerks T, Bork P (2014) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. doi:10.1093/nar/gku949
Bejerman N, Giolitti F, de Breuil S, Lenardon S (2010) Molecular characterization of Sunflower chlorotic mottle virus: a member of a distinct species in the genus Potyvirus. Arch Virol 155:1331–1335
Feng X, Poplawsky AR, Nikolaeva OV, Myers JR, Karasev AV (2014) Recombinants of Bean common mosaic virus (BCMV) and genetic determinants of BCMV involved in overcoming resistance in common bean. Phytopathology 104:786–793
Desbiez C, Lecoq H (2008) Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV, Potyvirus). Arch Virol 153:1749–17540
Bejerman N, Giolitti F, de Breuil S, Lenardon S (2013) Sequencing of two Sunflower chlorotic mottle virus isolates obtained from different natural hosts shed light on its evolutionary history. Virus Genes 46:105–110
Leyssen P, Charlier N, Lemey P, Billoir F, Vandamme AM, De Clercq E, de Lamballerie X, Neyts J (2002) Complete genome sequence, taxonomic assignment, and comparative analysis of the untranslated regions of the Modoc virus, a flavivirus with no known vector. Virology 293:125–140
Fargette D, Konate G, Fauquet C, Muller E, Peterschmitt M, Thresh JM (2006) Molecular ecology and emergence of tropical plant viruses. Annu Rev Phytopathol 44:235–260
Rodoni BC, Dale JL, Harding RM (1999) Characterization and expression of the coat protein-coding region of banana bract mosaic potyvirus, development of diagnostic assays and detection of the virus in banana plants from five countries in southeast Asia. Arch Virol 144:725–1737
Hu JS, Li HP, Barry K, Wang M (1995) Comparison of dot blot, ELISA, and RT-PCR assays for detection of two cucumber mosaic virus isolates infecting banana in Hawaii. Plant Dis 79:902–906
Fukuta S, Ohishi K, Yoshida K, Mizukami Y, Ishida A, Kanbe M (2004) Development of immunocapture reverse transcription loop-mediated isothermal amplification for the detection of tomato spotted wilt virus from chrysanthemum. J Virol Methods 121:49–55
Almasi MA, Moradi A, Nasiri J, Karami S, Nasiri M (2012) Assessment of performance ability of three diagnostic methods for detection of Potato Leafroll Virus (PLRV) using different visualizing systems. Appl Biochem Biotechnol. doi:10.1007/s12010-012-9818-1
Almasi MA, Hosseyni-Dehabadi SM, Aghapour-ojaghkandi M (2014) Comparison and evaluation of three diagnostic methods for detection of beet curly top virus in sugar beet using different visualizing systems. Appl Biochem Biotechnol 173:1836–18480
Acknowledgments
This work was supported in part by grants from the National Natural Science Foundation of China (31300118), the President Foundation of the Guangdong Academy of Agricultural Sciences (201306), the National Institute of Food and Agriculture, US Department of Agriculture, Hatch HAW09025-H (1001478), and the U.S. Department of Agriculture, Agricultural Research Service (58-5320-4-012).
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This study was funded by grants from the National Natural Science Foundation of China (31300118), the President Foundation of the Guangdong Academy of Agricultural Sciences (201306), the National Institute of Food and Agriculture, US Department of Agriculture, Hatch HAW09025-H (1001478), and the US Department of Agriculture, Agricultural Research Service (58-5320-4-012).
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Author Jingxin Zhang declares that he has no conflict of interest. Author Wayne Borth declares that he has no conflict of interest. Author Birun Lin declares that he has no conflict of interest. Author Kishore Dey declares that he has no conflict of interest. Author Michael Melzer declares that he has no conflict of interest. Author Huifang Shen declares that she has no conflict of interest. Author Xiaoming Pu declares that he has no conflict of interest. Author Dayuan Sun declares that he has no conflict of interest. Author John Hu declares that he has no conflict of interest.
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Zhang, J., Borth, W.B., Lin, B. et al. Deep sequencing of banana bract mosaic virus from flowering ginger (Alpinia purpurata) and development of an immunocapture RT-LAMP detection assay. Arch Virol 161, 1783–1795 (2016). https://doi.org/10.1007/s00705-016-2830-y
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DOI: https://doi.org/10.1007/s00705-016-2830-y