Genetic variability and evolutionary implications of RNA silencing suppressor genes in RNA1 of sweet potato chlorotic stunt virus isolates infecting sweetpotato and related wild species

The bipartite single-stranded RNA genome of Sweet potato chlorotic stunt virus (SPCSV, genus Crinivirus; Closteroviridae) encodes a Class 1 RNase III (RNase3), a putative hydrophobic protein (p7) and a 22-kDa protein (p22) from genes located in RNA1. RNase3 and p22 suppress RNA silencing, the basal...

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Veröffentlicht in:PloS one 2013-11, Vol.8 (11), p.e81479-e81479
Hauptverfasser: Tugume, Arthur K, Amayo, Robert, Weinheimer, Isabel, Mukasa, Settumba B, Rubaihayo, Patrick R, Valkonen, Jari P T
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container_issue 11
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container_title PloS one
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creator Tugume, Arthur K
Amayo, Robert
Weinheimer, Isabel
Mukasa, Settumba B
Rubaihayo, Patrick R
Valkonen, Jari P T
description The bipartite single-stranded RNA genome of Sweet potato chlorotic stunt virus (SPCSV, genus Crinivirus; Closteroviridae) encodes a Class 1 RNase III (RNase3), a putative hydrophobic protein (p7) and a 22-kDa protein (p22) from genes located in RNA1. RNase3 and p22 suppress RNA silencing, the basal antiviral defence mechanism in plants. RNase3 is sufficient to render sweetpotato (Ipomoea batatas) virus-susceptible and predisposes it to development of severe diseases following infection with unrelated virus. The incidence, strains and gene content of SPCSV infecting wild plant species have not been studied. Thirty SPCSV isolates were characterized from 10 wild Ipomoea species, Hewittia sublobata or Lepistemon owariensis (family Convolvulaceae) in Uganda and compared with 34 local SPCSV isolates infecting sweetpotatoes. All isolates belonged to the East African (EA) strain of SPCSV and contained RNase3 and p7, but p22 was not detected in six isolates. The three genes showed only limited genetic variability and the proteins were under purifying selection. SPCSV isolates lacking p22 synergized with Sweet potato feathery mottle virus (SPFMV, genus potyvirus; Potyviridae) and caused severe symptoms in co-infected sweetpotato plants. One SPCSV isolate enhanced accumulation of SPFMV, but no severe symptoms developed. A new whitefly-transmitted virus (KML33b) encoding an RNase3 homolog (
doi_str_mv 10.1371/journal.pone.0081479
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RNase3 and p22 suppress RNA silencing, the basal antiviral defence mechanism in plants. RNase3 is sufficient to render sweetpotato (Ipomoea batatas) virus-susceptible and predisposes it to development of severe diseases following infection with unrelated virus. The incidence, strains and gene content of SPCSV infecting wild plant species have not been studied. Thirty SPCSV isolates were characterized from 10 wild Ipomoea species, Hewittia sublobata or Lepistemon owariensis (family Convolvulaceae) in Uganda and compared with 34 local SPCSV isolates infecting sweetpotatoes. All isolates belonged to the East African (EA) strain of SPCSV and contained RNase3 and p7, but p22 was not detected in six isolates. The three genes showed only limited genetic variability and the proteins were under purifying selection. SPCSV isolates lacking p22 synergized with Sweet potato feathery mottle virus (SPFMV, genus potyvirus; Potyviridae) and caused severe symptoms in co-infected sweetpotato plants. One SPCSV isolate enhanced accumulation of SPFMV, but no severe symptoms developed. A new whitefly-transmitted virus (KML33b) encoding an RNase3 homolog (&lt;56% identity to SPCSV RNase3) able to suppresses sense-mediated RNA silencing was detected in I. sinensis. SPCSV isolates infecting wild species and sweetpotato in Uganda were genetically undifferentiated, suggesting inter-species transmission of SPCSV. Most isolates in Uganda contained p22, unlike SPCSV isolates characterized from other countries and continents. Enhanced accumulation of SPFMV and increased disease severity were found to be uncoupled phenotypic outcomes of RNase3-mediated viral synergism in sweetpotato. A second virus encoding an RNase3-like RNA silencing suppressor was detected. Overall, results provided many novel and important insights into evolutionary biology of SPCSV.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0081479</identifier><identifier>PMID: 24278443</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Accumulation ; Agriculture ; Amino Acid Sequence ; Bioinformatics ; Biological effects ; Biological evolution ; Closterovirus ; Continents ; Crinivirus - genetics ; Development and progression ; Environmental science ; Evolution &amp; development ; Evolution, Molecular ; Gene silencing ; Genes ; Genes, Suppressor ; Genetic engineering ; Genetic research ; Genetic variability ; Genetic Variation ; Genomes ; Genomics ; Health aspects ; Homology ; Hydrolases ; Hydrophobicity ; Infection ; Ipomoea ; Ipomoea batatas ; Ipomoea batatas - classification ; Ipomoea batatas - virology ; Molecular Sequence Data ; Phenotype ; Phylogenetics ; Phylogeny ; Plant Diseases - virology ; Plant species ; Plant virus diseases ; Plant viruses ; Plants (botany) ; Plants (Organisms) ; Potatoes ; Potyvirus ; Proteins ; Ribonuclease ; Ribonuclease III ; Ribonucleic acid ; RNA ; RNA viruses ; RNA, Viral - genetics ; RNA-mediated interference ; Selection, Genetic ; Sequence Alignment ; Serotyping ; Sweet potatoes ; Synergism ; Taste (Sense) ; Variability ; Viral Proteins - genetics ; Viruses</subject><ispartof>PloS one, 2013-11, Vol.8 (11), p.e81479-e81479</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Tugume et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/3.0/ (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>2013 Tugume et al 2013 Tugume et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-b49ee0ca7b34a5923ac5be081a5196329be624164d88eee32456d493d11953423</citedby><cites>FETCH-LOGICAL-c692t-b49ee0ca7b34a5923ac5be081a5196329be624164d88eee32456d493d11953423</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3838340/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3838340/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24278443$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Rao, A.L.N.</contributor><creatorcontrib>Tugume, Arthur K</creatorcontrib><creatorcontrib>Amayo, Robert</creatorcontrib><creatorcontrib>Weinheimer, Isabel</creatorcontrib><creatorcontrib>Mukasa, Settumba B</creatorcontrib><creatorcontrib>Rubaihayo, Patrick R</creatorcontrib><creatorcontrib>Valkonen, Jari P T</creatorcontrib><title>Genetic variability and evolutionary implications of RNA silencing suppressor genes in RNA1 of sweet potato chlorotic stunt virus isolates infecting sweetpotato and related wild species</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The bipartite single-stranded RNA genome of Sweet potato chlorotic stunt virus (SPCSV, genus Crinivirus; Closteroviridae) encodes a Class 1 RNase III (RNase3), a putative hydrophobic protein (p7) and a 22-kDa protein (p22) from genes located in RNA1. RNase3 and p22 suppress RNA silencing, the basal antiviral defence mechanism in plants. RNase3 is sufficient to render sweetpotato (Ipomoea batatas) virus-susceptible and predisposes it to development of severe diseases following infection with unrelated virus. The incidence, strains and gene content of SPCSV infecting wild plant species have not been studied. Thirty SPCSV isolates were characterized from 10 wild Ipomoea species, Hewittia sublobata or Lepistemon owariensis (family Convolvulaceae) in Uganda and compared with 34 local SPCSV isolates infecting sweetpotatoes. All isolates belonged to the East African (EA) strain of SPCSV and contained RNase3 and p7, but p22 was not detected in six isolates. The three genes showed only limited genetic variability and the proteins were under purifying selection. SPCSV isolates lacking p22 synergized with Sweet potato feathery mottle virus (SPFMV, genus potyvirus; Potyviridae) and caused severe symptoms in co-infected sweetpotato plants. One SPCSV isolate enhanced accumulation of SPFMV, but no severe symptoms developed. A new whitefly-transmitted virus (KML33b) encoding an RNase3 homolog (&lt;56% identity to SPCSV RNase3) able to suppresses sense-mediated RNA silencing was detected in I. sinensis. SPCSV isolates infecting wild species and sweetpotato in Uganda were genetically undifferentiated, suggesting inter-species transmission of SPCSV. Most isolates in Uganda contained p22, unlike SPCSV isolates characterized from other countries and continents. Enhanced accumulation of SPFMV and increased disease severity were found to be uncoupled phenotypic outcomes of RNase3-mediated viral synergism in sweetpotato. A second virus encoding an RNase3-like RNA silencing suppressor was detected. Overall, results provided many novel and important insights into evolutionary biology of SPCSV.</description><subject>Accumulation</subject><subject>Agriculture</subject><subject>Amino Acid Sequence</subject><subject>Bioinformatics</subject><subject>Biological effects</subject><subject>Biological evolution</subject><subject>Closterovirus</subject><subject>Continents</subject><subject>Crinivirus - genetics</subject><subject>Development and progression</subject><subject>Environmental science</subject><subject>Evolution &amp; development</subject><subject>Evolution, Molecular</subject><subject>Gene silencing</subject><subject>Genes</subject><subject>Genes, Suppressor</subject><subject>Genetic engineering</subject><subject>Genetic research</subject><subject>Genetic variability</subject><subject>Genetic Variation</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Homology</subject><subject>Hydrolases</subject><subject>Hydrophobicity</subject><subject>Infection</subject><subject>Ipomoea</subject><subject>Ipomoea batatas</subject><subject>Ipomoea batatas - classification</subject><subject>Ipomoea batatas - virology</subject><subject>Molecular Sequence Data</subject><subject>Phenotype</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Plant Diseases - virology</subject><subject>Plant species</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Plants (botany)</subject><subject>Plants (Organisms)</subject><subject>Potatoes</subject><subject>Potyvirus</subject><subject>Proteins</subject><subject>Ribonuclease</subject><subject>Ribonuclease III</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA viruses</subject><subject>RNA, Viral - genetics</subject><subject>RNA-mediated interference</subject><subject>Selection, Genetic</subject><subject>Sequence Alignment</subject><subject>Serotyping</subject><subject>Sweet potatoes</subject><subject>Synergism</subject><subject>Taste (Sense)</subject><subject>Variability</subject><subject>Viral Proteins - genetics</subject><subject>Viruses</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99u0zAUxiMEYmPwBggsISG4aLFjx4lvkKoJRqWJSePPreU4p60rNw6207FH4-1w2mxq0S6QLxInv-87PsfnZNlLgqeEluTD2vW-VXbauRamGFeEleJRdkoEzSc8x_TxwftJ9iyENcYFrTh_mp3kLC8rxuhp9ucCWohGo63yRtXGmniLVNsg2DrbR-Na5W-R2XTWaDVsA3ILdP11hoKx0GrTLlHou85DCM6jZXILyLQDQQYy3ABE1LmookN6ZZ13Q7QQ-zairfF9ooOzKu5kC9Bx5zioRtFwGA8D0aAbYxsUOtAGwvPsyULZAC_G51n24_On7-dfJpdXF_Pz2eVEc5HHSc0EANaqrClThcip0kUNqVyqIILTXNTAc0Y4a6oKAGjOCt4wQRtCREFZTs-y13vfzrogx6oHSRivBBUlYYmY74nGqbXsvNmkmkmnjNx9cH4plU9ZW5CYC6iFKjVThBGGFQYhmK6g4bzhIJLXxzFaX2-g0dBGr-yR6fGf1qzk0m0lrdJiOBm8Gw28-9VDiHJjggZrVQuu3507JwKTasjszT_ow9mN1FKlBNIduRRXD6ZyxsqK8CLfeU0foNJqYGN0atFFapdjwfsjQWIi_I5L1Ycg59-u_5-9-nnMvj1gV6BsXIWxlcMxyPag9i4ED4v7IhMshwm7q4YcJkyOE5Zkrw4v6F50N1L0L5i7JNc</recordid><startdate>20131122</startdate><enddate>20131122</enddate><creator>Tugume, Arthur K</creator><creator>Amayo, Robert</creator><creator>Weinheimer, Isabel</creator><creator>Mukasa, Settumba B</creator><creator>Rubaihayo, Patrick R</creator><creator>Valkonen, Jari P T</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20131122</creationdate><title>Genetic variability and evolutionary implications of RNA silencing suppressor genes in RNA1 of sweet potato chlorotic stunt virus isolates infecting sweetpotato and related wild species</title><author>Tugume, Arthur K ; Amayo, Robert ; Weinheimer, Isabel ; Mukasa, Settumba B ; Rubaihayo, Patrick R ; Valkonen, Jari P T</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-b49ee0ca7b34a5923ac5be081a5196329be624164d88eee32456d493d11953423</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Accumulation</topic><topic>Agriculture</topic><topic>Amino Acid Sequence</topic><topic>Bioinformatics</topic><topic>Biological effects</topic><topic>Biological evolution</topic><topic>Closterovirus</topic><topic>Continents</topic><topic>Crinivirus - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tugume, Arthur K</au><au>Amayo, Robert</au><au>Weinheimer, Isabel</au><au>Mukasa, Settumba B</au><au>Rubaihayo, Patrick R</au><au>Valkonen, Jari P T</au><au>Rao, A.L.N.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genetic variability and evolutionary implications of RNA silencing suppressor genes in RNA1 of sweet potato chlorotic stunt virus isolates infecting sweetpotato and related wild species</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-11-22</date><risdate>2013</risdate><volume>8</volume><issue>11</issue><spage>e81479</spage><epage>e81479</epage><pages>e81479-e81479</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The bipartite single-stranded RNA genome of Sweet potato chlorotic stunt virus (SPCSV, genus Crinivirus; Closteroviridae) encodes a Class 1 RNase III (RNase3), a putative hydrophobic protein (p7) and a 22-kDa protein (p22) from genes located in RNA1. RNase3 and p22 suppress RNA silencing, the basal antiviral defence mechanism in plants. RNase3 is sufficient to render sweetpotato (Ipomoea batatas) virus-susceptible and predisposes it to development of severe diseases following infection with unrelated virus. The incidence, strains and gene content of SPCSV infecting wild plant species have not been studied. Thirty SPCSV isolates were characterized from 10 wild Ipomoea species, Hewittia sublobata or Lepistemon owariensis (family Convolvulaceae) in Uganda and compared with 34 local SPCSV isolates infecting sweetpotatoes. All isolates belonged to the East African (EA) strain of SPCSV and contained RNase3 and p7, but p22 was not detected in six isolates. The three genes showed only limited genetic variability and the proteins were under purifying selection. SPCSV isolates lacking p22 synergized with Sweet potato feathery mottle virus (SPFMV, genus potyvirus; Potyviridae) and caused severe symptoms in co-infected sweetpotato plants. One SPCSV isolate enhanced accumulation of SPFMV, but no severe symptoms developed. A new whitefly-transmitted virus (KML33b) encoding an RNase3 homolog (&lt;56% identity to SPCSV RNase3) able to suppresses sense-mediated RNA silencing was detected in I. sinensis. SPCSV isolates infecting wild species and sweetpotato in Uganda were genetically undifferentiated, suggesting inter-species transmission of SPCSV. Most isolates in Uganda contained p22, unlike SPCSV isolates characterized from other countries and continents. Enhanced accumulation of SPFMV and increased disease severity were found to be uncoupled phenotypic outcomes of RNase3-mediated viral synergism in sweetpotato. A second virus encoding an RNase3-like RNA silencing suppressor was detected. Overall, results provided many novel and important insights into evolutionary biology of SPCSV.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24278443</pmid><doi>10.1371/journal.pone.0081479</doi><tpages>e81479</tpages><oa>free_for_read</oa></addata></record>
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subjects Accumulation
Agriculture
Amino Acid Sequence
Bioinformatics
Biological effects
Biological evolution
Closterovirus
Continents
Crinivirus - genetics
Development and progression
Environmental science
Evolution & development
Evolution, Molecular
Gene silencing
Genes
Genes, Suppressor
Genetic engineering
Genetic research
Genetic variability
Genetic Variation
Genomes
Genomics
Health aspects
Homology
Hydrolases
Hydrophobicity
Infection
Ipomoea
Ipomoea batatas
Ipomoea batatas - classification
Ipomoea batatas - virology
Molecular Sequence Data
Phenotype
Phylogenetics
Phylogeny
Plant Diseases - virology
Plant species
Plant virus diseases
Plant viruses
Plants (botany)
Plants (Organisms)
Potatoes
Potyvirus
Proteins
Ribonuclease
Ribonuclease III
Ribonucleic acid
RNA
RNA viruses
RNA, Viral - genetics
RNA-mediated interference
Selection, Genetic
Sequence Alignment
Serotyping
Sweet potatoes
Synergism
Taste (Sense)
Variability
Viral Proteins - genetics
Viruses
title Genetic variability and evolutionary implications of RNA silencing suppressor genes in RNA1 of sweet potato chlorotic stunt virus isolates infecting sweetpotato and related wild species
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