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...
Gespeichert in:
Veröffentlicht in: | PLoS pathogens 2022-04, Vol.18 (4), p.e1010448-e1010448 |
---|---|
Hauptverfasser: | , , , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | e1010448 |
---|---|
container_issue | 4 |
container_start_page | e1010448 |
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. |
doi_str_mv | 10.1371/journal.ppat.1010448 |
format | Article |
fullrecord | <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_2665134554</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A702006938</galeid><doaj_id>oai_doaj_org_article_abb95e94488b4abda38b1be78887fe76</doaj_id><sourcerecordid>A702006938</sourcerecordid><originalsourceid>FETCH-LOGICAL-c699t-7d00873033e05f3eb09766a0f0338d82c63512db5d7e698394aea643303886143</originalsourceid><addsrcrecordid>eNqVk99u0zAUxiMEYmPwBggicQMSLXYd_7tBqiZglaohDbi2Thyn9ZTawXYKfQJeG4d20zrthvgi9vHv--xzrFMULzGaYsLxh2s_BAfdtO8hTTHCqKrEo-IUU0omnPDq8Z35SfEsxmuEKkwwe1qcEJpniMvT4s-8dOZXtyvNxoSVdasSun4NEZLpOptMCW1rdIplDS6Psh6cXu_K5Ptya8MQy2D6zmpI1rv3ZQrgog623y-jvbqcl33wzaDHSAmu2TMbG-MYqHcl9GvbxOfFkxa6aF4c_mfFj8-fvp9fTJZfvyzO58uJZlKmCW8QEpwgQgyiLTE1kpwxQG2OiEbMNCMUz5qaNtwwKYiswACrSFYIwXBFzorXe9--81EdahjVjDGKSUXpSCz2ROPhWvXBbiDslAer_gV8WCkIyerOKKhrSY3MhRd1BXUDRNS4NlwIwVvDWfb6eDhtqDem0cbl7Lsj0-MdZ9dq5bdKokrSGcoGk73B-p7sYr5UPcRkhqAQYVQSyrc4828PBwb_czAxqVxpnZ8SnPHDmGcl88dn493e3EMfrsaBWkFO2LrW53vq0VTNOZohxCQRmZo-QOXRmI3V3pnW5viR4N2RIDPJ_E4rGGJUi29X_8FeHrPVntXBxxhMe1s0jNTYNjdJqrFt1KFtsuzV3Xe6Fd30CfkLxGcT5w</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2665134554</pqid></control><display><type>article</type><title>A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids</title><source>Public Library of Science (PLoS) Journals Open Access</source><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><source>PubMed Central Open Access</source><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</creator><creatorcontrib>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</creatorcontrib><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.</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 & 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2022 Guyot et al 2022 Guyot et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c699t-7d00873033e05f3eb09766a0f0338d82c63512db5d7e698394aea643303886143</citedby><cites>FETCH-LOGICAL-c699t-7d00873033e05f3eb09766a0f0338d82c63512db5d7e698394aea643303886143</cites><orcidid>0000-0003-2308-393X ; 0000-0002-0105-3919 ; 0000-0003-4486-2449 ; 0000-0002-5920-4775 ; 0000-0001-5486-0098</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9049520/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9049520/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35413079$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://pasteur.hal.science/pasteur-03659357$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Guyot, Valentin</creatorcontrib><creatorcontrib>Rajeswaran, Rajendran</creatorcontrib><creatorcontrib>Chu, Huong Cam</creatorcontrib><creatorcontrib>Karthikeyan, Chockalingam</creatorcontrib><creatorcontrib>Laboureau, Nathalie</creatorcontrib><creatorcontrib>Galzi, Serge</creatorcontrib><creatorcontrib>Mukwa, Lyna F T</creatorcontrib><creatorcontrib>Krupovic, Mart</creatorcontrib><creatorcontrib>Kumar, P Lava</creatorcontrib><creatorcontrib>Iskra-Caruana, Marie-Line</creatorcontrib><creatorcontrib>Pooggin, Mikhail M</creatorcontrib><title>A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><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.</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 & 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 - genetics</subject><subject>Sequence analysis</subject><subject>siRNA</subject><subject>Transcription</subject><subject>Transcriptomes</subject><subject>Viral proteins</subject><subject>Virology</subject><subject>Viruses</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk99u0zAUxiMEYmPwBggicQMSLXYd_7tBqiZglaohDbi2Thyn9ZTawXYKfQJeG4d20zrthvgi9vHv--xzrFMULzGaYsLxh2s_BAfdtO8hTTHCqKrEo-IUU0omnPDq8Z35SfEsxmuEKkwwe1qcEJpniMvT4s-8dOZXtyvNxoSVdasSun4NEZLpOptMCW1rdIplDS6Psh6cXu_K5Ptya8MQy2D6zmpI1rv3ZQrgog623y-jvbqcl33wzaDHSAmu2TMbG-MYqHcl9GvbxOfFkxa6aF4c_mfFj8-fvp9fTJZfvyzO58uJZlKmCW8QEpwgQgyiLTE1kpwxQG2OiEbMNCMUz5qaNtwwKYiswACrSFYIwXBFzorXe9--81EdahjVjDGKSUXpSCz2ROPhWvXBbiDslAer_gV8WCkIyerOKKhrSY3MhRd1BXUDRNS4NlwIwVvDWfb6eDhtqDem0cbl7Lsj0-MdZ9dq5bdKokrSGcoGk73B-p7sYr5UPcRkhqAQYVQSyrc4828PBwb_czAxqVxpnZ8SnPHDmGcl88dn493e3EMfrsaBWkFO2LrW53vq0VTNOZohxCQRmZo-QOXRmI3V3pnW5viR4N2RIDPJ_E4rGGJUi29X_8FeHrPVntXBxxhMe1s0jNTYNjdJqrFt1KFtsuzV3Xe6Fd30CfkLxGcT5w</recordid><startdate>20220412</startdate><enddate>20220412</enddate><creator>Guyot, Valentin</creator><creator>Rajeswaran, Rajendran</creator><creator>Chu, Huong Cam</creator><creator>Karthikeyan, Chockalingam</creator><creator>Laboureau, Nathalie</creator><creator>Galzi, Serge</creator><creator>Mukwa, Lyna F T</creator><creator>Krupovic, Mart</creator><creator>Kumar, P Lava</creator><creator>Iskra-Caruana, Marie-Line</creator><creator>Pooggin, Mikhail M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><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></search><sort><creationdate>20220412</creationdate><title>A newly emerging alphasatellite affects banana bunchy top virus replication, transcription, siRNA production and transmission by aphids</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c699t-7d00873033e05f3eb09766a0f0338d82c63512db5d7e698394aea643303886143</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Aphid transmission factor</topic><topic>Aphididae</topic><topic>Aphids</topic><topic>Aphids - genetics</topic><topic>Babuvirus</topic><topic>Babuvirus - genetics</topic><topic>Banana</topic><topic>Binding sites</topic><topic>Biology and life sciences</topic><topic>Bunchy top</topic><topic>Cloning</topic><topic>Coat protein</topic><topic>Cost benefit analysis</topic><topic>Deoxyribonucleic acid</topic><topic>Disease transmission</topic><topic>Diseases and pests</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA viruses</topic><topic>DNA, Viral</topic><topic>DNA, Viral - genetics</topic><topic>Environmental aspects</topic><topic>Flowers & plants</topic><topic>Fruits</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Helper viruses</topic><topic>Host-virus relationships</topic><topic>Identification and classification</topic><topic>Insects</topic><topic>Leaves</topic><topic>Life Sciences</topic><topic>Microbiology and Parasitology</topic><topic>Movement protein</topic><topic>Musa</topic><topic>Musaceae</topic><topic>Nanoviridae</topic><topic>New genera</topic><topic>Nucleotides</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Plant Diseases</topic><topic>Plant viruses</topic><topic>Proteins</topic><topic>Relative abundance</topic><topic>Replication</topic><topic>Research and Analysis Methods</topic><topic>RNA polymerase</topic><topic>RNA, Small Interfering</topic><topic>RNA, Small Interfering - genetics</topic><topic>Sequence analysis</topic><topic>siRNA</topic><topic>Transcription</topic><topic>Transcriptomes</topic><topic>Viral proteins</topic><topic>Virology</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guyot, Valentin</creatorcontrib><creatorcontrib>Rajeswaran, Rajendran</creatorcontrib><creatorcontrib>Chu, Huong Cam</creatorcontrib><creatorcontrib>Karthikeyan, Chockalingam</creatorcontrib><creatorcontrib>Laboureau, Nathalie</creatorcontrib><creatorcontrib>Galzi, Serge</creatorcontrib><creatorcontrib>Mukwa, Lyna F T</creatorcontrib><creatorcontrib>Krupovic, Mart</creatorcontrib><creatorcontrib>Kumar, P Lava</creatorcontrib><creatorcontrib>Iskra-Caruana, Marie-Line</creatorcontrib><creatorcontrib>Pooggin, Mikhail M</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - 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> |
fulltext | fulltext |
identifier | ISSN: 1553-7374 |
ispartof | PLoS pathogens, 2022-04, Vol.18 (4), p.e1010448-e1010448 |
issn | 1553-7374 1553-7366 1553-7374 |
language | eng |
recordid | cdi_plos_journals_2665134554 |
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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T16%3A46%3A18IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20newly%20emerging%20alphasatellite%20affects%20banana%20bunchy%20top%20virus%20replication,%20transcription,%20siRNA%20production%20and%20transmission%20by%20aphids&rft.jtitle=PLoS%20pathogens&rft.au=Guyot,%20Valentin&rft.date=2022-04-12&rft.volume=18&rft.issue=4&rft.spage=e1010448&rft.epage=e1010448&rft.pages=e1010448-e1010448&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1010448&rft_dat=%3Cgale_plos_%3EA702006938%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2665134554&rft_id=info:pmid/35413079&rft_galeid=A702006938&rft_doaj_id=oai_doaj_org_article_abb95e94488b4abda38b1be78887fe76&rfr_iscdi=true |