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A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids

dc.contributor.authorGuyot, V.
dc.contributor.authorRajeswaran, R.
dc.contributor.authorChu, H.C.
dc.contributor.authorKarthikeyan, C.
dc.contributor.authorLaboureau, N.
dc.contributor.authorGalzi, S.
dc.contributor.authorMukwa, L.
dc.contributor.authorKrupovic, M.
dc.contributor.authorKumar, P.L.
dc.contributor.authorIskra-Caruana, M.L.
dc.contributor.authorPooggin, M.
dc.date.accessioned2022-05-20T15:14:11Z
dc.date.available2022-05-20T15:14:11Z
dc.date.issued2022
dc.identifier.citationGuyot, V., Rajeswaran, R., Chu, H.C., Karthikeyan, C., Laboureau, N., Galzi, S., ... & Pooggin, M. (2022). A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids. PLoS Pathogens, 18(4), 1-40.
dc.identifier.issn1553-7366
dc.identifier.urihttps://hdl.handle.net/20.500.12478/7472
dc.description.abstractBanana bunchy top virus (BBTV) is a six-component ssDNA virus (genus Babuvirus, family Nanoviridae) transmitted by aphids, infecting monocots (mainly species in the family Musaceae) and likely originating from South-East Asia where it is frequently associated with self-replicating alphasatellites. Illumina sequencing analysis of banana aphids and leaf samples from Africa revealed an alphasatellite that should be classified in a new genus, phylogenetically related to alphasatellites of nanoviruses infecting dicots. Alphasatellite DNA was encapsidated by BBTV coat protein and accumulated at high levels in plants and aphids, thereby reducing helper virus loads, altering relative abundance (formula) of viral genome components and interfering with virus transmission by aphids. BBTV and alphasatellite clones infected dicot Nicotiana benthamiana, followed by recovery and symptomless persistence of alphasatellite, and BBTV replication protein (Rep), but not alphasatellite Rep, induced leaf chlorosis. Transcriptome sequencing revealed 21, 22 and 24 nucleotide small interfering (si)RNAs covering both strands of the entire viral genome, monodirectional Pol II transcription units of viral mRNAs and pervasive transcription of each component and alphasatellite in both directions, likely generating double-stranded precursors of viral siRNAs. Consistent with the latter hypothesis, viral DNA formulas with and without alphasatellite resembled viral siRNA formulas but not mRNA formulas. Alphasatellite decreased transcription efficiency of DNA-N encoding a putative aphid transmission factor and increased relative siRNA production rates from Rep- and movement protein-encoding components. Alphasatellite itself spawned the most abundant siRNAs and had the lowest mRNA transcription rate. Collectively, following African invasion, BBTV got associated with an alphasatellite likely originating from a dicot plant and interfering with BBTV replication and transmission. Molecular analysis of virus-infected banana plants revealed new features of viral DNA transcription and siRNA biogenesis, both affected by alphasatellite. Costs and benefits of alphasatellite association with helper viruses are discussed.
dc.description.sponsorshipCGIAR Research Program on Roots, Tubers and Bananas
dc.description.sponsorshipCGIAR Trust Fund
dc.format.extent1-40
dc.language.isoen_US
dc.subjectRna
dc.subjectBananas
dc.subjectViruses
dc.subjectPlant Diseases
dc.subjectDna
dc.subjectAphididae
dc.titleA newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids
dc.typeJournal Article
cg.contributor.crpMaize
cg.contributor.crpRoots, Tubers and Bananas
cg.contributor.affiliationUniversity of Montpellier
cg.contributor.affiliationUniversite Pedagogique Nationale, Democratic Republic of the Congo
cg.contributor.affiliationUniversite Paris Cite
cg.contributor.affiliationInternational Institute of Tropical Agriculture
cg.contributor.affiliationCentre de Coopération Internationale en Recherche Agronomique pour le Développement
cg.coverage.regionAfrica
cg.coverage.regionCentral Africa
cg.coverage.countryDemocratic Republic of the Congo
cg.coverage.hubHeadquarters and Western Africa Hub
cg.researchthemePlant Production and Health
cg.identifier.bibtexciteidGUYOT:2022
cg.isijournalISI Journal
cg.authorship.typesCGIAR and developing country institute
cg.iitasubjectAgronomy
cg.iitasubjectBanana
cg.iitasubjectDisease Control
cg.iitasubjectFood Security
cg.iitasubjectPlant Breeding
cg.iitasubjectPlant Diseases
cg.iitasubjectPlant Health
cg.iitasubjectPlant Production
cg.journalPLoS Pathogens
cg.notesOpen Access Journal; Published online: 12 Apr 2022
cg.accessibilitystatusOpen Access
cg.reviewstatusPeer Review
cg.usagerightslicenseCreative Commons Attribution 4.0 (CC BY 0.0)
cg.targetaudienceScientists
cg.identifier.doihttps://dx.doi.org/10.1371/journal.ppat.1010448
cg.iitaauthor.identifierP. Lava Kumar: 0000-0003-4388-6510
cg.futureupdate.requiredNo
cg.identifier.issue4
cg.identifier.volume18


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