A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids
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. I...
| Autores principales: | , , , , , , , , , , |
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| Formato: | Journal Article |
| Lenguaje: | Inglés |
| Publicado: |
2022
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| Materias: | |
| Acceso en línea: | https://hdl.handle.net/10568/119608 |
| _version_ | 1855535195399127040 |
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| author | Guyot, V. Rajeswaran, R. Chu, H.C. Karthikeyan, C. Laboureau, N. Galzi, S. Mukwa, L. Krupovic, M. Kumar, P. Lava Iskra-Caruana, M.L. Pooggin, M. |
| author_browse | Chu, H.C. Galzi, S. Guyot, V. Iskra-Caruana, M.L. Karthikeyan, C. Krupovic, M. Kumar, P. Lava Laboureau, N. Mukwa, L. Pooggin, M. Rajeswaran, R. |
| author_facet | Guyot, V. Rajeswaran, R. Chu, H.C. Karthikeyan, C. Laboureau, N. Galzi, S. Mukwa, L. Krupovic, M. Kumar, P. Lava Iskra-Caruana, M.L. Pooggin, M. |
| author_sort | Guyot, V. |
| collection | Repository of Agricultural Research Outputs (CGSpace) |
| 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. |
| format | Journal Article |
| id | CGSpace119608 |
| institution | CGIAR Consortium |
| language | Inglés |
| publishDate | 2022 |
| publishDateRange | 2022 |
| publishDateSort | 2022 |
| record_format | dspace |
| spelling | CGSpace1196082025-11-11T10:41:31Z A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids Guyot, V. Rajeswaran, R. Chu, H.C. Karthikeyan, C. Laboureau, N. Galzi, S. Mukwa, L. Krupovic, M. Kumar, P. Lava Iskra-Caruana, M.L. Pooggin, M. rna bananas viruses plant diseases dna aphididae 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. 2022 2022-05-20T15:14:31Z 2022-05-20T15:14:31Z Journal Article https://hdl.handle.net/10568/119608 en Open Access application/pdf Guyot, 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. |
| spellingShingle | rna bananas viruses plant diseases dna aphididae Guyot, V. Rajeswaran, R. Chu, H.C. Karthikeyan, C. Laboureau, N. Galzi, S. Mukwa, L. Krupovic, M. Kumar, P. Lava Iskra-Caruana, M.L. Pooggin, M. A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids |
| title | A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids |
| title_full | A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids |
| title_fullStr | A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids |
| title_full_unstemmed | A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids |
| title_short | A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids |
| title_sort | newly emerging alphasatellite affects banana bunchy top virus replication transcription sirna production and transmission by aphids |
| topic | rna bananas viruses plant diseases dna aphididae |
| url | https://hdl.handle.net/10568/119608 |
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