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

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    Journal Article (4.142Mb)
    Date
    2022
    Author
    Guyot, V.
    Rajeswaran, R.
    Chu, H.C.
    Karthikeyan, C.
    Laboureau, N.
    Galzi, S.
    Mukwa, L.
    Krupovic, M.
    Kumar, P.L.
    Iskra-Caruana, M.L.
    Pooggin, M.
    Type
    Journal Article
    Review Status
    Peer Review
    Target Audience
    Scientists
    Metadata
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    Abstract/Description
    Banana 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.
    https://dx.doi.org/10.1371/journal.ppat.1010448
    Multi standard citation
    Permanent link to this item
    https://hdl.handle.net/20.500.12478/7472
    IITA Authors ORCID
    P. Lava Kumarhttps://orcid.org/0000-0003-4388-6510
    Digital Object Identifier (DOI)
    https://dx.doi.org/10.1371/journal.ppat.1010448
    Research Themes
    Plant Production and Health
    IITA Subjects
    Agronomy; Banana; Disease Control; Food Security; Plant Breeding; Plant Diseases; Plant Health; Plant Production
    Agrovoc Terms
    Rna; Bananas; Viruses; Plant Diseases; Dna; Aphididae
    Regions
    Africa; Central Africa
    Countries
    Democratic Republic of the Congo
    Hubs
    Headquarters and Western Africa Hub
    Journals
    PLoS Pathogens
    Collections
    • Journal and Journal Articles4501
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