Isolation and Characterization of Pepper Genes Interacting with the CMV-P1 Helicase Domain
Cucumber mosaic virus (CMV) is a destructive pathogen affecting Capsicum annuum (pepper) production. The pepper Cmr1 gene confers resistance to most CMV strains, but is overcome by CMV-P1 in a process dependent on the CMV-P1 RNA1 helicase domain (P1 helicase). Here, to identify host factors involved...
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| creator | Choi, Yoomi Kang, Min-Young Lee, Joung-Ho Kang, Won-Hee Hwang, JeeNa Kwon, Jin-Kyung Kang, Byoung-Cheorl |
| description | Cucumber mosaic virus (CMV) is a destructive pathogen affecting Capsicum annuum (pepper) production. The pepper Cmr1 gene confers resistance to most CMV strains, but is overcome by CMV-P1 in a process dependent on the CMV-P1 RNA1 helicase domain (P1 helicase). Here, to identify host factors involved in CMV-P1 infection in pepper, a yeast two-hybrid library derived from a C. annuum 'Bukang' cDNA library was screened, producing a total of 76 potential clones interacting with the P1 helicase. Beta-galactosidase filter lift assay, PCR screening, and sequencing analysis narrowed the candidates to 10 genes putatively involved in virus infection. The candidate host genes were silenced in Nicotiana benthamiana plants that were then inoculated with CMV-P1 tagged with the green fluorescent protein (GFP). Plants silenced for seven of the genes showed development comparable to N. benthamiana wild type, whereas plants silenced for the other three genes showed developmental defects including stunting and severe distortion. Silencing formate dehydrogenase and calreticulin-3 precursor led to reduced virus accumulation. Formate dehydrogenase-silenced plants showed local infection in inoculated leaves, but not in upper (systemic) leaves. In the calreticulin-3 precursor-silenced plants, infection was not observed in either the inoculated or the upper leaves. Our results demonstrate that formate dehydrogenase and calreticulin-3 precursor are required for CMV-P1 infection. |
| doi_str_mv | 10.1371/journal.pone.0146320 |
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The pepper Cmr1 gene confers resistance to most CMV strains, but is overcome by CMV-P1 in a process dependent on the CMV-P1 RNA1 helicase domain (P1 helicase). Here, to identify host factors involved in CMV-P1 infection in pepper, a yeast two-hybrid library derived from a C. annuum 'Bukang' cDNA library was screened, producing a total of 76 potential clones interacting with the P1 helicase. Beta-galactosidase filter lift assay, PCR screening, and sequencing analysis narrowed the candidates to 10 genes putatively involved in virus infection. The candidate host genes were silenced in Nicotiana benthamiana plants that were then inoculated with CMV-P1 tagged with the green fluorescent protein (GFP). Plants silenced for seven of the genes showed development comparable to N. benthamiana wild type, whereas plants silenced for the other three genes showed developmental defects including stunting and severe distortion. Silencing formate dehydrogenase and calreticulin-3 precursor led to reduced virus accumulation. Formate dehydrogenase-silenced plants showed local infection in inoculated leaves, but not in upper (systemic) leaves. In the calreticulin-3 precursor-silenced plants, infection was not observed in either the inoculated or the upper leaves. Our results demonstrate that formate dehydrogenase and calreticulin-3 precursor are required for CMV-P1 infection.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0146320</identifier><identifier>PMID: 26751216</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agrobacterium - metabolism ; beta-Galactosidase - metabolism ; Calreticulin ; Calreticulin - genetics ; Capsicum - genetics ; Capsicum annuum ; Cloning ; CMR1 gene ; Cucumovirus - enzymology ; Cucumovirus - genetics ; Dehydrogenase ; Dehydrogenases ; Diseases and pests ; DNA helicase ; DNA, Complementary - metabolism ; Endoplasmic reticulum ; Fluorescence ; Formate dehydrogenase ; Formate Dehydrogenases - genetics ; Galactosidase ; Gene Expression Regulation, Plant ; Gene Library ; Gene sequencing ; Gene Silencing ; Genes ; Genes, Plant ; Genetic aspects ; Genomics ; Green fluorescent protein ; Green Fluorescent Proteins - metabolism ; Helicases ; Infections ; Kinases ; Leaves ; Life sciences ; Medical screening ; Nicotiana benthamiana ; Peppers ; Physiological aspects ; Physiology ; Plant Diseases - genetics ; Plant Leaves - metabolism ; Plant mitochondria ; Plant sciences ; Plant virus diseases ; Plant viruses ; Plants ; Polymerase Chain Reaction ; Precursors ; Protein Binding ; Protein Structure, Tertiary ; Proteins ; RNA Helicases - metabolism ; RNA polymerase ; Sequence Analysis, DNA ; Tobacco ; Two-Hybrid System Techniques ; Vegetables ; Viruses ; Yeast ; Yeasts ; β-Galactosidase</subject><ispartof>PloS one, 2016-01, Vol.11 (1), p.e0146320-e0146320</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Choi 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>2016 Choi et al 2016 Choi et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-d584084c5a5cb22e7489c024322c88eea613260d63b242d0ba01aea0d397ce073</citedby><cites>FETCH-LOGICAL-c692t-d584084c5a5cb22e7489c024322c88eea613260d63b242d0ba01aea0d397ce073</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/PMC4709182/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4709182/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26751216$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Choi, Yoomi</creatorcontrib><creatorcontrib>Kang, Min-Young</creatorcontrib><creatorcontrib>Lee, Joung-Ho</creatorcontrib><creatorcontrib>Kang, Won-Hee</creatorcontrib><creatorcontrib>Hwang, JeeNa</creatorcontrib><creatorcontrib>Kwon, Jin-Kyung</creatorcontrib><creatorcontrib>Kang, Byoung-Cheorl</creatorcontrib><title>Isolation and Characterization of Pepper Genes Interacting with the CMV-P1 Helicase Domain</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Cucumber mosaic virus (CMV) is a destructive pathogen affecting Capsicum annuum (pepper) production. The pepper Cmr1 gene confers resistance to most CMV strains, but is overcome by CMV-P1 in a process dependent on the CMV-P1 RNA1 helicase domain (P1 helicase). Here, to identify host factors involved in CMV-P1 infection in pepper, a yeast two-hybrid library derived from a C. annuum 'Bukang' cDNA library was screened, producing a total of 76 potential clones interacting with the P1 helicase. Beta-galactosidase filter lift assay, PCR screening, and sequencing analysis narrowed the candidates to 10 genes putatively involved in virus infection. The candidate host genes were silenced in Nicotiana benthamiana plants that were then inoculated with CMV-P1 tagged with the green fluorescent protein (GFP). Plants silenced for seven of the genes showed development comparable to N. benthamiana wild type, whereas plants silenced for the other three genes showed developmental defects including stunting and severe distortion. Silencing formate dehydrogenase and calreticulin-3 precursor led to reduced virus accumulation. Formate dehydrogenase-silenced plants showed local infection in inoculated leaves, but not in upper (systemic) leaves. In the calreticulin-3 precursor-silenced plants, infection was not observed in either the inoculated or the upper leaves. Our results demonstrate that formate dehydrogenase and calreticulin-3 precursor are required for CMV-P1 infection.</description><subject>Agrobacterium - metabolism</subject><subject>beta-Galactosidase - metabolism</subject><subject>Calreticulin</subject><subject>Calreticulin - genetics</subject><subject>Capsicum - genetics</subject><subject>Capsicum annuum</subject><subject>Cloning</subject><subject>CMR1 gene</subject><subject>Cucumovirus - enzymology</subject><subject>Cucumovirus - genetics</subject><subject>Dehydrogenase</subject><subject>Dehydrogenases</subject><subject>Diseases and pests</subject><subject>DNA helicase</subject><subject>DNA, Complementary - metabolism</subject><subject>Endoplasmic reticulum</subject><subject>Fluorescence</subject><subject>Formate dehydrogenase</subject><subject>Formate Dehydrogenases - genetics</subject><subject>Galactosidase</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Library</subject><subject>Gene sequencing</subject><subject>Gene Silencing</subject><subject>Genes</subject><subject>Genes, Plant</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Green fluorescent protein</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Helicases</subject><subject>Infections</subject><subject>Kinases</subject><subject>Leaves</subject><subject>Life sciences</subject><subject>Medical screening</subject><subject>Nicotiana benthamiana</subject><subject>Peppers</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Plant Diseases - genetics</subject><subject>Plant Leaves - metabolism</subject><subject>Plant mitochondria</subject><subject>Plant sciences</subject><subject>Plant virus diseases</subject><subject>Plant viruses</subject><subject>Plants</subject><subject>Polymerase Chain Reaction</subject><subject>Precursors</subject><subject>Protein Binding</subject><subject>Protein Structure, Tertiary</subject><subject>Proteins</subject><subject>RNA Helicases - metabolism</subject><subject>RNA polymerase</subject><subject>Sequence Analysis, DNA</subject><subject>Tobacco</subject><subject>Two-Hybrid System Techniques</subject><subject>Vegetables</subject><subject>Viruses</subject><subject>Yeast</subject><subject>Yeasts</subject><subject>β-Galactosidase</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk01v1DAQhiMEoqXwDxBEQkJw2MVfcZxLpWqBdqWiVnz0wMWadSa7rrL2Yid8_Xq8bFptUA_IB1vj531tj2ey7CklU8pL-uba98FBO914h1NCheSM3MsOacXZRDLC7--tD7JHMV4TUnAl5cPsgMmyoIzKw-zrPPoWOutdDq7OZysIYDoM9vcu6Jv8EjcbDPkpOoz53KXNRFi3zH_YbpV3K8xnH64mlzQ_w9YaiJi_9Wuw7nH2oIE24pNhPsq-vH_3eXY2Ob84nc9OzidGVqyb1IUSRAlTQGEWjGEpVGUIE5wxoxQiSMqZJLXkCyZYTRZAKCCQmlelQVLyo-z5znfT-qiHtERNy6Ioq0JKlYj5jqg9XOtNsGsIv7QHq_8GfFhqCJ01LWpa8KRrVEVQiZLUFaiaUiGkqZCWpUxex8Np_WKNtUHXBWhHpuMdZ1d66b_r5FZRxZLBq8Eg-G89xk6vbTTYtuDQ99t7S6IKQYoqoS_-Qe9-3UAtIT3Ausanc83WVJ8IXklChBKJmt5BpVHj2ppUQ41N8ZHg9UiQmA5_dkvoY9TzTx__n724GrMv99gVQtutUg3223KLY1DsQBN8jAGb2yRTorctcJMNvW0BPbRAkj3b_6Bb0U3N8z8rVP4q</recordid><startdate>20160111</startdate><enddate>20160111</enddate><creator>Choi, Yoomi</creator><creator>Kang, Min-Young</creator><creator>Lee, Joung-Ho</creator><creator>Kang, Won-Hee</creator><creator>Hwang, JeeNa</creator><creator>Kwon, Jin-Kyung</creator><creator>Kang, Byoung-Cheorl</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>AEUYN</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>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160111</creationdate><title>Isolation and Characterization of Pepper Genes Interacting with the CMV-P1 Helicase Domain</title><author>Choi, Yoomi ; Kang, Min-Young ; Lee, Joung-Ho ; Kang, Won-Hee ; Hwang, JeeNa ; Kwon, Jin-Kyung ; Kang, Byoung-Cheorl</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-d584084c5a5cb22e7489c024322c88eea613260d63b242d0ba01aea0d397ce073</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Agrobacterium - metabolism</topic><topic>beta-Galactosidase - metabolism</topic><topic>Calreticulin</topic><topic>Calreticulin - genetics</topic><topic>Capsicum - genetics</topic><topic>Capsicum annuum</topic><topic>Cloning</topic><topic>CMR1 gene</topic><topic>Cucumovirus - enzymology</topic><topic>Cucumovirus - genetics</topic><topic>Dehydrogenase</topic><topic>Dehydrogenases</topic><topic>Diseases and pests</topic><topic>DNA helicase</topic><topic>DNA, Complementary - metabolism</topic><topic>Endoplasmic reticulum</topic><topic>Fluorescence</topic><topic>Formate dehydrogenase</topic><topic>Formate Dehydrogenases - genetics</topic><topic>Galactosidase</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Library</topic><topic>Gene sequencing</topic><topic>Gene Silencing</topic><topic>Genes</topic><topic>Genes, Plant</topic><topic>Genetic aspects</topic><topic>Genomics</topic><topic>Green fluorescent protein</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Helicases</topic><topic>Infections</topic><topic>Kinases</topic><topic>Leaves</topic><topic>Life sciences</topic><topic>Medical screening</topic><topic>Nicotiana benthamiana</topic><topic>Peppers</topic><topic>Physiological aspects</topic><topic>Physiology</topic><topic>Plant Diseases - 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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>Choi, Yoomi</au><au>Kang, Min-Young</au><au>Lee, Joung-Ho</au><au>Kang, Won-Hee</au><au>Hwang, JeeNa</au><au>Kwon, Jin-Kyung</au><au>Kang, Byoung-Cheorl</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Isolation and Characterization of Pepper Genes Interacting with the CMV-P1 Helicase Domain</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-01-11</date><risdate>2016</risdate><volume>11</volume><issue>1</issue><spage>e0146320</spage><epage>e0146320</epage><pages>e0146320-e0146320</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Cucumber mosaic virus (CMV) is a destructive pathogen affecting Capsicum annuum (pepper) production. The pepper Cmr1 gene confers resistance to most CMV strains, but is overcome by CMV-P1 in a process dependent on the CMV-P1 RNA1 helicase domain (P1 helicase). Here, to identify host factors involved in CMV-P1 infection in pepper, a yeast two-hybrid library derived from a C. annuum 'Bukang' cDNA library was screened, producing a total of 76 potential clones interacting with the P1 helicase. Beta-galactosidase filter lift assay, PCR screening, and sequencing analysis narrowed the candidates to 10 genes putatively involved in virus infection. The candidate host genes were silenced in Nicotiana benthamiana plants that were then inoculated with CMV-P1 tagged with the green fluorescent protein (GFP). Plants silenced for seven of the genes showed development comparable to N. benthamiana wild type, whereas plants silenced for the other three genes showed developmental defects including stunting and severe distortion. Silencing formate dehydrogenase and calreticulin-3 precursor led to reduced virus accumulation. Formate dehydrogenase-silenced plants showed local infection in inoculated leaves, but not in upper (systemic) leaves. In the calreticulin-3 precursor-silenced plants, infection was not observed in either the inoculated or the upper leaves. Our results demonstrate that formate dehydrogenase and calreticulin-3 precursor are required for CMV-P1 infection.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26751216</pmid><doi>10.1371/journal.pone.0146320</doi><tpages>e0146320</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2016-01, Vol.11 (1), p.e0146320-e0146320 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1755795668 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Agrobacterium - metabolism beta-Galactosidase - metabolism Calreticulin Calreticulin - genetics Capsicum - genetics Capsicum annuum Cloning CMR1 gene Cucumovirus - enzymology Cucumovirus - genetics Dehydrogenase Dehydrogenases Diseases and pests DNA helicase DNA, Complementary - metabolism Endoplasmic reticulum Fluorescence Formate dehydrogenase Formate Dehydrogenases - genetics Galactosidase Gene Expression Regulation, Plant Gene Library Gene sequencing Gene Silencing Genes Genes, Plant Genetic aspects Genomics Green fluorescent protein Green Fluorescent Proteins - metabolism Helicases Infections Kinases Leaves Life sciences Medical screening Nicotiana benthamiana Peppers Physiological aspects Physiology Plant Diseases - genetics Plant Leaves - metabolism Plant mitochondria Plant sciences Plant virus diseases Plant viruses Plants Polymerase Chain Reaction Precursors Protein Binding Protein Structure, Tertiary Proteins RNA Helicases - metabolism RNA polymerase Sequence Analysis, DNA Tobacco Two-Hybrid System Techniques Vegetables Viruses Yeast Yeasts β-Galactosidase |
| title | Isolation and Characterization of Pepper Genes Interacting with the CMV-P1 Helicase Domain |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-06T16%3A52%3A25IST&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=Isolation%20and%20Characterization%20of%20Pepper%20Genes%20Interacting%20with%20the%20CMV-P1%20Helicase%20Domain&rft.jtitle=PloS%20one&rft.au=Choi,%20Yoomi&rft.date=2016-01-11&rft.volume=11&rft.issue=1&rft.spage=e0146320&rft.epage=e0146320&rft.pages=e0146320-e0146320&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0146320&rft_dat=%3Cgale_plos_%3EA439600484%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=1755795668&rft_id=info:pmid/26751216&rft_galeid=A439600484&rft_doaj_id=oai_doaj_org_article_153755f890e8470d9a8d11446c9e1776&rfr_iscdi=true |