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...

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Veröffentlicht in:PLoS pathogens 2022-04, Vol.18 (4), p.e1010448-e1010448
Hauptverfasser: Guyot, Valentin, Rajeswaran, Rajendran, Chu, Huong Cam, Karthikeyan, Chockalingam, Laboureau, Nathalie, Galzi, Serge, Mukwa, Lyna F T, Krupovic, Mart, Kumar, P Lava, Iskra-Caruana, Marie-Line, Pooggin, Mikhail M
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container_issue 4
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container_title PLoS pathogens
container_volume 18
creator Guyot, Valentin
Rajeswaran, Rajendran
Chu, Huong Cam
Karthikeyan, Chockalingam
Laboureau, Nathalie
Galzi, Serge
Mukwa, Lyna F T
Krupovic, Mart
Kumar, P Lava
Iskra-Caruana, Marie-Line
Pooggin, Mikhail M
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.
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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.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1010448</identifier><identifier>PMID: 35413079</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Aphid transmission factor ; Aphididae ; Aphids ; Aphids - genetics ; Babuvirus ; Babuvirus - genetics ; Banana ; Binding sites ; Biology and life sciences ; Bunchy top ; Cloning ; Coat protein ; Cost benefit analysis ; Deoxyribonucleic acid ; Disease transmission ; Diseases and pests ; DNA ; DNA methylation ; DNA viruses ; DNA, Viral ; DNA, Viral - genetics ; Environmental aspects ; Flowers &amp; plants ; Fruits ; Gene expression ; Genetic aspects ; Genomes ; Helper viruses ; Host-virus relationships ; Identification and classification ; Insects ; Leaves ; Life Sciences ; Microbiology and Parasitology ; Movement protein ; Musa ; Musaceae ; Nanoviridae ; New genera ; Nucleotides ; Phylogenetics ; Phylogeny ; Plant Diseases ; Plant viruses ; Proteins ; Relative abundance ; Replication ; Research and Analysis Methods ; RNA polymerase ; RNA, Small Interfering ; RNA, Small Interfering - genetics ; Sequence analysis ; siRNA ; Transcription ; Transcriptomes ; Viral proteins ; Virology ; Viruses</subject><ispartof>PLoS pathogens, 2022-04, Vol.18 (4), p.e1010448-e1010448</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Guyot et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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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.</description><subject>Animals</subject><subject>Aphid transmission factor</subject><subject>Aphididae</subject><subject>Aphids</subject><subject>Aphids - genetics</subject><subject>Babuvirus</subject><subject>Babuvirus - genetics</subject><subject>Banana</subject><subject>Binding sites</subject><subject>Biology and life sciences</subject><subject>Bunchy top</subject><subject>Cloning</subject><subject>Coat protein</subject><subject>Cost benefit analysis</subject><subject>Deoxyribonucleic acid</subject><subject>Disease transmission</subject><subject>Diseases and pests</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA viruses</subject><subject>DNA, Viral</subject><subject>DNA, Viral - genetics</subject><subject>Environmental aspects</subject><subject>Flowers &amp; plants</subject><subject>Fruits</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Helper viruses</subject><subject>Host-virus relationships</subject><subject>Identification and classification</subject><subject>Insects</subject><subject>Leaves</subject><subject>Life Sciences</subject><subject>Microbiology and Parasitology</subject><subject>Movement protein</subject><subject>Musa</subject><subject>Musaceae</subject><subject>Nanoviridae</subject><subject>New genera</subject><subject>Nucleotides</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Plant Diseases</subject><subject>Plant viruses</subject><subject>Proteins</subject><subject>Relative abundance</subject><subject>Replication</subject><subject>Research and Analysis Methods</subject><subject>RNA polymerase</subject><subject>RNA, Small Interfering</subject><subject>RNA, Small Interfering - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guyot, Valentin</au><au>Rajeswaran, Rajendran</au><au>Chu, Huong Cam</au><au>Karthikeyan, Chockalingam</au><au>Laboureau, Nathalie</au><au>Galzi, Serge</au><au>Mukwa, Lyna F T</au><au>Krupovic, Mart</au><au>Kumar, P Lava</au><au>Iskra-Caruana, Marie-Line</au><au>Pooggin, Mikhail M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2022-04-12</date><risdate>2022</risdate><volume>18</volume><issue>4</issue><spage>e1010448</spage><epage>e1010448</epage><pages>e1010448-e1010448</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>35413079</pmid><doi>10.1371/journal.ppat.1010448</doi><tpages>e1010448</tpages><orcidid>https://orcid.org/0000-0003-2308-393X</orcidid><orcidid>https://orcid.org/0000-0002-0105-3919</orcidid><orcidid>https://orcid.org/0000-0003-4486-2449</orcidid><orcidid>https://orcid.org/0000-0002-5920-4775</orcidid><orcidid>https://orcid.org/0000-0001-5486-0098</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1553-7374
ispartof PLoS pathogens, 2022-04, Vol.18 (4), p.e1010448-e1010448
issn 1553-7374
1553-7366
1553-7374
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source Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; PubMed Central Open Access
subjects Animals
Aphid transmission factor
Aphididae
Aphids
Aphids - genetics
Babuvirus
Babuvirus - genetics
Banana
Binding sites
Biology and life sciences
Bunchy top
Cloning
Coat protein
Cost benefit analysis
Deoxyribonucleic acid
Disease transmission
Diseases and pests
DNA
DNA methylation
DNA viruses
DNA, Viral
DNA, Viral - genetics
Environmental aspects
Flowers & plants
Fruits
Gene expression
Genetic aspects
Genomes
Helper viruses
Host-virus relationships
Identification and classification
Insects
Leaves
Life Sciences
Microbiology and Parasitology
Movement protein
Musa
Musaceae
Nanoviridae
New genera
Nucleotides
Phylogenetics
Phylogeny
Plant Diseases
Plant viruses
Proteins
Relative abundance
Replication
Research and Analysis Methods
RNA polymerase
RNA, Small Interfering
RNA, Small Interfering - genetics
Sequence analysis
siRNA
Transcription
Transcriptomes
Viral proteins
Virology
Viruses
title A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids
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