Identification of Divergent Isolates of Banana Mild Mosaic Virus and Development of a New Diagnostic Primer to Improve Detection

Hanafi, Marwa; Tahzima, Rachid; BEN KAAB, Sofiene; Tamisier, lucie; Roux, Nicolas; Massart, Sébastien

doi:10.3390/pathogens9121045

Article (Scientific journals)

Identification of Divergent Isolates of Banana Mild Mosaic Virus and Development of a New Diagnostic Primer to Improve Detection

Hanafi, Marwa; Tahzima, Rachid; BEN KAAB, Sofiene et al.

2020 • In Pathogens

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/255167

DOI
10.3390/pathogens9121045

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Hanafi et al.,2020.pdf

Publisher postprint (1.01 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

high throughput sequencing (HTS); diagnostic; BanMMV; Betaflexiviridae; primers; novel isolates; plant virus; total RNA

Abstract :

[en] Banana mild mosaic virus (BanMMV) (Betaflexiviridae, Quinvirinae, unassigned species) is a filamentous virus belonging to the Betaflexiviridae family. It infects Musa spp. with a very wide geographic distribution. The genome variability of plant viruses, including the members of the Betaflexiviridae family, makes their molecular detection by specific primers particularly challenging. During routine indexing of the Musa germplasm accessions, a discrepancy was observed between electron microscopy and immunocapture (IC) reverse transcription (RT) polymerase chain reaction (PCR) test results for one asymptomatic accession. Filamentous viral particles were observed while molecular tests failed to amplify any fragment. The accession underwent high-throughput sequencing and two complete genomes of BanMMV with 75.3% of identity were assembled. Based on these sequences and on the 54 coat protein sequences available from GenBank, a new forward primer, named BanMMV CP9, compatible with Poty1, an oligodT reverse primer already used in diagnostics, was designed. A retrospective analysis of 110 different germplasm accessions from diverse origins was conducted, comparing BanMMCP2 and BanMMV CP9 primers. Of these 110 accessions, 16 tested positive with both BanMMCP2 and BanMMV CP9, 3 were positive with only BanMMCP2 and 2 tested positive with only BanMMV CP9. Otherwise, 89 were negative with the two primers and free of flexuous virions. Sanger sequencing was performed from purified PCR products in order to confirm the amplification of the BanMMV sequence for the five accessions with contrasting results. It is highly recommended to use the two primers successively to improve the inclusiveness of the protocol.

Disciplines :

Biotechnology

Author, co-author :

Hanafi, Marwa ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Tahzima, Rachid ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

BEN KAAB, Sofiene; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Tamisier, lucie ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Roux, Nicolas; Consultative Group on International Agricultural Research, 34090 Montpellier, France

Massart, Sébastien ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Language :

English

Title :

Identification of Divergent Isolates of Banana Mild Mosaic Virus and Development of a New Diagnostic Primer to Improve Detection

Publication date :

12 December 2020

Journal title :

Pathogens

eISSN :

2076-0817

Publisher :

Molecular Diversity Preservation International (MDPI), Basel, Switzerland

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 15 January 2021

Statistics

Number of views

116 (16 by ULiège)

Number of downloads

56 (6 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Kouakou, T.K.; Caroline, D.C.; Therese, A.A.; Ludivine, L.; Olivier, P.; Sebastien, M.; Philippe, L.; Mohamed, H.J. Prevalence of viruses infecting plantain (Musa sp., AAB genome) in the major growing regions in Cote dIvoire. Afr. J. Agric. Res. 2016, 11, 4532–4541, doi:10.5897/ajar2016.11421.
Christelová, P.; De Langhe, E.; Hřibová, E.; Čížková, J.; Sardos, J.; Hušáková, M.; Van den houwe, I.; Sutanto, A.; Kepler, A.K.; Swennen, R.; et al. Molecular and cytological characterization of the global Musa germplasm collection provides insights into the treasure of banana diversity. Biodivers. Conserv. 2017, 26, 801–824, doi:10.1007/s10531-016-1273-9.
Teycheney, P.Y.; Laboureau, N.; Iskra-Caruana, M.L.; Candresse, T. High genetic variability and evidence for plant-to-plant transfer of Banana mild mosaic virus. J. Gen. Virol. 2005, 86, 3179–3187, doi:10.1099/vir.0.81197-0.
Gambley, C.F.; Thomas, J.E. Molecular characterisation of Banana mild mosaic virus, a new filamentous virus in Musa spp. Arch. Virol. 2001, 146, 1369–1379, doi:10.1007/s007050170097.
Schrader, G.; Unger, J. Plant quarantine as a measure against invasive alien species: The framework of the International Plant Protection Convention and the plant health regulations in the European Union. 2003, 5, 357–364.
Buko, D.H.; Gedebo, A.; Spetz, C. An update of sweet potato viral disease incidence and spread in Ethiopia. 2020, 16, 1116–1126, doi:10.5897/AJAR2020.14918.
Le Provost, G.; Iskra-Caruana, M.L.; Acina, I.; Teycheney, P.Y. Improved detection of episomal Banana streak viruses by multiplex immunocapture PCR. J. Virol. Methods 2006, 137, 7–13, doi:10.1016/j.jviromet.2006.05.021.
Thomas, J.E. Technical Guidelines for The Safe Movement of Musa Germplasm; Bioversity International: Rome, Italy, 2015; ISBN 9789292550349.
Zarghani, S.N.; Hily, J.M.; Glasa, M.; Marais, A.; Wetzel, T.; Faure, C.; Vigne, E.; Velt, A.; Lemaire, O.; Boursiquot, J.M.; et al. Grapevine virus T diversity as revealed by full-length genome sequences assembled from high-throughput sequence data. PLoS ONE 2018, 13, 1–17, doi:10.1371/journal.pone.0206010.
Diaz-lara, A.; Golino, D.; Preece, J.E.; Al, M. Development of RT-PCR degenerate primers to overcome the high genetic diversity of grapevine virus T. J. Virol. Methods 2020, 282, 113883, doi:10.1016/j.jviromet.2020.113883.
Da Silva, L.A.; Oliveira, A.S.; Melo, F.L.; Ardisson-Araújo, D.M.P.; Resende, F.V.; Resende, R.O.; Ribeiro, B.M. A new virus found in garlic virus complex is a member of possible novel genus of the family Betaflexiviridae (order Tymovirales). PeerJ 2019, 2019, 1–11, doi:10.7717/peerj.6285.
Baker, R.; Caffier, D.; Choiseul, J.W.; Clercq, P.; De; Gerowitt, B.; Karadjova, O.E.; Lövei, G.; Oude, A.; Makowski, D.; Manceau, C.; et al. Pest risk assessment made by France on Banana bract mosaic virus considered by France as harmful in French overseas departments of French Guiana, Guadeloupe, Martinique and Réunion—Scientific Opinion of the Panel on Plant Health. EFSA J. 2008, 6, 1–21, doi:10.2903/j.efsa.2008.651.
Teycheney, P.Y.; Acina, I.; Lockhart, B.E.L.; Candresse, T. Detection of Banana mild mosaic virus and Banana virus X by polyvalent degenerate oligonucleotide RT-PCR (PDO-RT-PCR). J. Virol. Methods 2007, 142, 41–49, doi:10.1016/j.jviromet.2007.01.004.
Fidan, H.; Koç, G. Occurrence, ecology and phylogeny of banana streak badnavirus (BSV) and cucumber mosaic cucumovirus (CMV) in musa SP. production areas of the mediterranean coastline of Turkey. Appl. Ecol. Environ. Res. 2019, 17, 5935, doi:10.15666/aeer/1703_59355951.
Foissac, X.; Svanella-Dumas, L.; Gentit, P.; Dulucq, M.J.; Marais, A.; Candresse, T. Polyvalent degenerate oligonucleotides reverse transcription-polymerase chain reaction: A polyvalent detection and characterization tool for trichoviruses, capilloviruses, and foveaviruses. Phytopathology 2005, 95, 617–625, doi:10.1094/PHYTO-95-0617.
Tedersoo, L.; Cleary, M. High—Throughput identification and diagnostics of pathogens and pests: Overview and practical recommendations. 2019, 47–76, doi:10.1111/1755-0998.12959.
Yang, I.C.; Hafner, G.J.; Revill, P.A.; Dale, J.L.; Harding, R.M. Sequence diversity of South Pacific isolates of Taro bacilliform virus and the development of a PCR-based diagnostic test. Arch. Virol. 2003, 148, 1957– 1968, doi:10.1007/s00705-003-0163-0.
Olmos, A.; Boonham, N.; Candresse, T.; Gentit, P.; Giovani, B.; Kutnjak, D.; Liefting, L.; Maree, H.J.; Minafra, A.; Moreira, A.; et al. High-throughput sequencing technologies for plant pest diagnosis: Challenges and opportunities. EPPO Bull. 2018, 48, 219–224, doi:10.1111/epp.12472.
Massart, S.; Candresse, T.; Gil, J.; Lacomme, C.; Predajna, L.; Ravnikar, M.; Reynard, J.S.; Rumbou, A.; Saldarelli, P.; Škoric, D.; et al. A framework for the evaluation of biosecurity, commercial, regulatory, and scientific impacts of plant viruses and viroids identified by NGS technologies. Front. Microbiol. 2017, 8, doi:10.3389/fmicb.2017.00045.
Villamor, D.E.V.; Mekuria, T.A.; Pillai, S.S.; Eastwell, K.C. High-Throughput Sequencing Identifies Novel Viruses in Nectarine: Insights to the Etiology of Stem-Pitting Disease. Phytopathology 2016, 106, 519–527.
Massart, S.; Olmos, A.; Jijakli, H.; Candresse, T. Current impact and future directions of high throughput sequencing in plant virus diagnostics. Virus Res. 2014, 188, 90–96.
Jones, S.; Baizan-Edge, A.; MacFarlane, S.; Torrance, L. Viral diagnostics in plants using next generation sequencing: Computational analysis in practice. Front. Plant Sci. 2017, 8, doi:10.3389/fpls.2017.01770.
De Clerck, C.; Crew, K.; Van den houwe, I.; McMichael, L.; Berhal, C.; Lassois, L.; Jijakli, M.H.; Roux, N.; Thomas, J.; Massart, S. Lessons learned from the virus indexing of Musa germplasm: Insights from a multiyear collaboration. Ann. Appl. Biol. 2017, 171, 15–27, doi:10.1111/aab.12353.
Sharman, M.; Thomas, J.E.; Dietzgen, R.G. Development of a multiplex immunocapture PCR with colourimetric detection for viruses of banana. J. Virol. Methods 2000, 89, 75–88, doi:10.1016/S0166-0934(00)00204-4.
Gazel, M.; Roumi, V.; Ördek, K.; Maclot, F.; Massart, S.; Çağlayan, K. Identification and molecular characterization of a novel foveavirus from Rubus spp. in Turkey. Virus Res. 2020, 286, 26–29, doi:10.1016/j.virusres.2020.198078.
Prime, G. User Manual Geneious Prime. Data Base 2012, 3304, 1–148.
Buzkan, N.; Chiumenti, M.; Massart, S.; Sarpkaya, K.; Karadağ, S.; Minafra, A. A new emaravirus discovered in Pistacia from Turkey. Virus Res. 2019, 263, 159–163, doi:10.1016/j.virusres.2019.01.012.
Komínek, P.; Massart, S.; Pham, K.; van Leeuwen, P.; Komínková, M. Characterisation of a novel virus infecting orchids of the genus Pleione. Virus Res. 2019, 261, 56–59, doi:10.1016/j.virusres.2018.12.009.
da Silva, W.; Kutnjak, D.; Xu, Y.; Xu, Y.; Giovannoni, J.; Elena, S.F.; Gray, S. Transmission modes affect the population structure of potato virus Y in potato. PLoS Pathog. 2020, 16, e1008608, doi:10.1371/journal.ppat.1008608.
Loukanov, A.; El Allaoui, N.; Omor, A.; Elmadani, F.Z.; Bouayad, K.; Seiichiro, N. Journal P. J. Neurol. Sci. 2020, 116544, doi:10.1016/j.meegid.2020.104627.
Albuquerque, L.C.; Inoue-Nagata, A.K.; Pinheiro, B.; Resende, R.O.; Moriones, E.; Navas-Castillo, J. Genetic diversity and recombination analysis of sweepoviruses from Brazil. Virol. J. 2012, 9, doi:10.1186/1743-422X-9-241.
Mavridis, K.; Wipf, N.; Medves, S.; Erquiaga, I.; Müller, P.; Vontas, J. Rapid multiplex gene expression assays for monitoring metabolic resistance in the major malaria vector Anopheles gambiae 06 Biological Sciences 0604 Genetics. Parasites Vectors 2019, 12, 1–13, doi:10.1186/s13071-018-3253-2.
Çağlayan, K.; Roumi, V.; Gazel, M.; Elçi, E.; Acioğlu, M.; Plesko, I.M.; Reynard, J.S.; Maclot, F.; Massart, S. Identification and characterization of a novel Robigovirus species from sweet cherry in turkey. Pathogens 2019, 8, 1–12, doi:10.3390/pathogens8020057.
Ii, P.; Positive, T.; Single, S.; Rna, S. Betaflexiviridae. Virus Taxon. 2012, 920–941, doi:10.1016/b978-0-12-384684-6.00078-1.
Meena, R.P.; Prabha, K.; Baranwal, V.K. Development of RT-PCR degenerate primers for the detection of two mandariviruses infecting citrus cultivars in India. J. Virol. Methods 2020, 275, 113753, doi:10.1016/j.jviromet.2019.113753.
Caruana, M.L.; Galzi, S. Identification of uncharacterised filamentous viral particles on banana plants. Acta Hortic. 1998, 490, 323–335, doi:10.17660/actahortic.1998.490.32.
Kesanakurti, P.; Belton, M.; Saeed, H.; Rast, H.; Boyes, I.; Rott, M. Comparative analysis of cherry virus A genome sequences assembled from deep sequencing data. Arch. Virol. 2017, 162, 2821–2828, doi:10.1007/s00705-017-3394-1.
Lauring, A.S.; Andino, R. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 2010, 6, 1–8, doi:10.1371/journal.ppat.1001005.
Jones, D.R. Handbook of Diseases of Banana, Abacá and Enset; CABI: Wallingford, UK, 2019.
Selvarajan, R.; Balasubramanian, V. First report of banana bract mosaic virus in banana in Assam, India. J. Plant Pathol. 2017, 99, 534.
Noll, L.W.; Stoy, C.P.A.; Wang, Y.; Porter, E.G.; Lu, N.; Liu, X.; Burklund, A.; Peddireddi, L.; Hanzlicek, G.; Henningson, J.; et al. Development of a nested PCR assay for detection of Streptococcus equi subspecies equi in clinical equine specimens and comparison with a qPCR assay. J. Microbiol. Methods 2020, 172, 105887, doi:10.1016/j.mimet.2020.105887.
Rames, E.K.; Macdonald, J. Rapid assessment of viral water quality using a novel recombinase polymerase amplification test for human adenovirus. Appl. Microbiol. Biotechnol. 2019, 103, 8115–8125, doi:10.1007/s00253-019-10077-w.
Ben-Dov, E.; Shapiro, O.H.; Siboni, N.; Kushmaro, A. Advantage of using inosine at the 3′ termini of 16S rRNA gene universal primers for the study of microbial diversity. Appl. Environ. Microbiol. 2006, 72, 6902– 6906, doi:10.1128/AEM.00849-06.
Ben-Dov, E.; Kushmaro, A. Inosine at Different Primer Positions to Study Structure and Diversity of Prokaryotic Populations. Curr. Issues Mol. Biol. 2015, 17, 53–56, doi:10.21775/cimb.017.053.
Wright, D.J.; Force, C.R.; Znosko, B.M. Stability of RNA duplexes containing inosine·cytosine pairs. Nucleic Acids Res. 2018, 46, 12099–12108, doi:10.1093/nar/gky907.