Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad‐spectrum virus resistance
Summary Recessive strain‐specific resistance to a number of plant viruses in the Potyvirus genus has been found to be based on mutations in the eukaryotic translation initiation factor 4E (eIF4E) and its isoform, eIF(iso)4E. We identified three copies of eIF(iso)4E in a number of Brassica rapa lines...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2014-01, Vol.77 (2), p.261-268 |
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creator | Nellist, Charlotte F. Qian, Wei Jenner, Carol E. Moore, Jonathan D. Zhang, Shujiang Wang, Xiaowu Briggs, William H. Barker, Guy C. Sun, Rifei Walsh, John A. |
description | Summary
Recessive strain‐specific resistance to a number of plant viruses in the Potyvirus genus has been found to be based on mutations in the eukaryotic translation initiation factor 4E (eIF4E) and its isoform, eIF(iso)4E. We identified three copies of eIF(iso)4E in a number of Brassica rapa lines. Here we report broad‐spectrum resistance to the potyvirus Turnip mosaic virus (TuMV) due to a natural mechanism based on the mis‐splicing of the eIF(iso)4E allele in some TuMV‐resistant B. rapa var. pekinensis lines. Of the splice variants, the most common results in a stop codon in intron 1 and a much truncated, non‐functional protein. The existence of multiple copies has enabled redundancy in the host plant's translational machinery, resulting in diversification and emergence of the resistance. Deployment of the resistance is complicated by the presence of multiple copies of the gene. Our data suggest that in the B. rapa subspecies trilocularis, TuMV appears to be able to use copies of eIF(iso)4E at two loci. Transformation of different copies of eIF(iso)4E from a resistant B. rapa line into an eIF(iso)4E knockout line of Arabidopsis thaliana proved misleading because it showed that, when expressed ectopically, TuMV could use multiple copies which was not the case in the resistant B. rapa line. The inability of TuMV to access multiple copies of eIF(iso)4E in B. rapa and the broad spectrum of the resistance suggest it may be durable. |
doi_str_mv | 10.1111/tpj.12389 |
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Recessive strain‐specific resistance to a number of plant viruses in the Potyvirus genus has been found to be based on mutations in the eukaryotic translation initiation factor 4E (eIF4E) and its isoform, eIF(iso)4E. We identified three copies of eIF(iso)4E in a number of Brassica rapa lines. Here we report broad‐spectrum resistance to the potyvirus Turnip mosaic virus (TuMV) due to a natural mechanism based on the mis‐splicing of the eIF(iso)4E allele in some TuMV‐resistant B. rapa var. pekinensis lines. Of the splice variants, the most common results in a stop codon in intron 1 and a much truncated, non‐functional protein. The existence of multiple copies has enabled redundancy in the host plant's translational machinery, resulting in diversification and emergence of the resistance. Deployment of the resistance is complicated by the presence of multiple copies of the gene. Our data suggest that in the B. rapa subspecies trilocularis, TuMV appears to be able to use copies of eIF(iso)4E at two loci. Transformation of different copies of eIF(iso)4E from a resistant B. rapa line into an eIF(iso)4E knockout line of Arabidopsis thaliana proved misleading because it showed that, when expressed ectopically, TuMV could use multiple copies which was not the case in the resistant B. rapa line. The inability of TuMV to access multiple copies of eIF(iso)4E in B. rapa and the broad spectrum of the resistance suggest it may be durable.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.12389</identifier><identifier>PMID: 24274163</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis thaliana ; Brassica rapa ; Brassica rapa - genetics ; Brassica rapa - metabolism ; Brassica rapa - virology ; broad‐spectrum virus resistance ; Chinese cabbage ; Codon, Terminator ; eIF(iso)4E ; Eukaryotes ; Eukaryotic Initiation Factors - metabolism ; Genes, Plant ; Genes, Recessive ; Introns ; mis‐splicing ; Molecular Sequence Data ; Plant diseases ; Plant pathology ; Plant resistance ; Potyvirus ; Rape plants ; RNA Splicing ; Turnip mosaic virus</subject><ispartof>The Plant journal : for cell and molecular biology, 2014-01, Vol.77 (2), p.261-268</ispartof><rights>2013 The Authors The Plant Journal © 2013 John Wiley & Sons Ltd</rights><rights>2013 The Authors The Plant Journal © 2013 John Wiley & Sons Ltd.</rights><rights>Copyright © 2014 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4879-44441474947d01e2c7b9b015c9583abb339dfd98a131c5a66d076ff5a0a6c68c3</citedby><cites>FETCH-LOGICAL-c4879-44441474947d01e2c7b9b015c9583abb339dfd98a131c5a66d076ff5a0a6c68c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.12389$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.12389$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24274163$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nellist, Charlotte F.</creatorcontrib><creatorcontrib>Qian, Wei</creatorcontrib><creatorcontrib>Jenner, Carol E.</creatorcontrib><creatorcontrib>Moore, Jonathan D.</creatorcontrib><creatorcontrib>Zhang, Shujiang</creatorcontrib><creatorcontrib>Wang, Xiaowu</creatorcontrib><creatorcontrib>Briggs, William H.</creatorcontrib><creatorcontrib>Barker, Guy C.</creatorcontrib><creatorcontrib>Sun, Rifei</creatorcontrib><creatorcontrib>Walsh, John A.</creatorcontrib><title>Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad‐spectrum virus resistance</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Recessive strain‐specific resistance to a number of plant viruses in the Potyvirus genus has been found to be based on mutations in the eukaryotic translation initiation factor 4E (eIF4E) and its isoform, eIF(iso)4E. We identified three copies of eIF(iso)4E in a number of Brassica rapa lines. Here we report broad‐spectrum resistance to the potyvirus Turnip mosaic virus (TuMV) due to a natural mechanism based on the mis‐splicing of the eIF(iso)4E allele in some TuMV‐resistant B. rapa var. pekinensis lines. Of the splice variants, the most common results in a stop codon in intron 1 and a much truncated, non‐functional protein. The existence of multiple copies has enabled redundancy in the host plant's translational machinery, resulting in diversification and emergence of the resistance. Deployment of the resistance is complicated by the presence of multiple copies of the gene. Our data suggest that in the B. rapa subspecies trilocularis, TuMV appears to be able to use copies of eIF(iso)4E at two loci. Transformation of different copies of eIF(iso)4E from a resistant B. rapa line into an eIF(iso)4E knockout line of Arabidopsis thaliana proved misleading because it showed that, when expressed ectopically, TuMV could use multiple copies which was not the case in the resistant B. rapa line. The inability of TuMV to access multiple copies of eIF(iso)4E in B. rapa and the broad spectrum of the resistance suggest it may be durable.</description><subject>Arabidopsis thaliana</subject><subject>Brassica rapa</subject><subject>Brassica rapa - genetics</subject><subject>Brassica rapa - metabolism</subject><subject>Brassica rapa - virology</subject><subject>broad‐spectrum virus resistance</subject><subject>Chinese cabbage</subject><subject>Codon, Terminator</subject><subject>eIF(iso)4E</subject><subject>Eukaryotes</subject><subject>Eukaryotic Initiation Factors - metabolism</subject><subject>Genes, Plant</subject><subject>Genes, Recessive</subject><subject>Introns</subject><subject>mis‐splicing</subject><subject>Molecular Sequence Data</subject><subject>Plant diseases</subject><subject>Plant pathology</subject><subject>Plant resistance</subject><subject>Potyvirus</subject><subject>Rape plants</subject><subject>RNA Splicing</subject><subject>Turnip mosaic virus</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks1uFSEUgInR2NvqwhcwJG5s4rTDwMCw1Mbf1OiiJu4mZ4BpuXJhBOaau_MRfCVfxSeR22ldmBjPAsjhOx8h5yD0iNQnpMRpntYnpKGdvINWhPK2ooR-votWteR1JRhpDtBhSuu6JoJydh8dNKwpaU5X6Of72WU7OYNVmKxJOIzYzF8g7kK2CucIPjnINnhsvc12OY6gcoippPCLCClZBTjCBPsL62yGbHA0evYavNo9w8bD4Ky_xNpuTUx2LAXXonwVw3x5hbcQ7e0rOE3Oqj0NXuMhBtC_vv9Ik1E5zhu8tXFOxZ5sysVuHqB7I7hkHt7sR-jTq5cXZ2-q8w-v3549P68U64SsWAnCBJNM6JqYRolBDjVplWw7CsNAqdSjlh0QSlQLnOta8HFsoQaueKfoEXq6eKcYvs4m5X5jkzLOgTdhTj1pCWONbCT9P8ok77qysII--Qtdhzn68pFCiZYIIjpZqOOFUjGkFM3YT9FuSpN6Uvf7EejLCPTXI1DYxzfGedgY_Ye87XkBThfgm3Vm929Tf_Hx3aL8Dd4GwN8</recordid><startdate>201401</startdate><enddate>201401</enddate><creator>Nellist, Charlotte F.</creator><creator>Qian, Wei</creator><creator>Jenner, Carol E.</creator><creator>Moore, Jonathan D.</creator><creator>Zhang, Shujiang</creator><creator>Wang, Xiaowu</creator><creator>Briggs, William H.</creator><creator>Barker, Guy C.</creator><creator>Sun, Rifei</creator><creator>Walsh, John A.</creator><general>Blackwell Publishing Ltd</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7U9</scope><scope>H94</scope><scope>7X8</scope></search><sort><creationdate>201401</creationdate><title>Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad‐spectrum virus resistance</title><author>Nellist, Charlotte F. ; Qian, Wei ; Jenner, Carol E. ; Moore, Jonathan D. ; Zhang, Shujiang ; Wang, Xiaowu ; Briggs, William H. ; Barker, Guy C. ; Sun, Rifei ; Walsh, John A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4879-44441474947d01e2c7b9b015c9583abb339dfd98a131c5a66d076ff5a0a6c68c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Arabidopsis thaliana</topic><topic>Brassica rapa</topic><topic>Brassica rapa - genetics</topic><topic>Brassica rapa - metabolism</topic><topic>Brassica rapa - virology</topic><topic>broad‐spectrum virus resistance</topic><topic>Chinese cabbage</topic><topic>Codon, Terminator</topic><topic>eIF(iso)4E</topic><topic>Eukaryotes</topic><topic>Eukaryotic Initiation Factors - metabolism</topic><topic>Genes, Plant</topic><topic>Genes, Recessive</topic><topic>Introns</topic><topic>mis‐splicing</topic><topic>Molecular Sequence Data</topic><topic>Plant diseases</topic><topic>Plant pathology</topic><topic>Plant resistance</topic><topic>Potyvirus</topic><topic>Rape plants</topic><topic>RNA Splicing</topic><topic>Turnip mosaic virus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nellist, Charlotte F.</creatorcontrib><creatorcontrib>Qian, Wei</creatorcontrib><creatorcontrib>Jenner, Carol E.</creatorcontrib><creatorcontrib>Moore, Jonathan D.</creatorcontrib><creatorcontrib>Zhang, Shujiang</creatorcontrib><creatorcontrib>Wang, Xiaowu</creatorcontrib><creatorcontrib>Briggs, William H.</creatorcontrib><creatorcontrib>Barker, Guy C.</creatorcontrib><creatorcontrib>Sun, Rifei</creatorcontrib><creatorcontrib>Walsh, John A.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nellist, Charlotte F.</au><au>Qian, Wei</au><au>Jenner, Carol E.</au><au>Moore, Jonathan D.</au><au>Zhang, Shujiang</au><au>Wang, Xiaowu</au><au>Briggs, William H.</au><au>Barker, Guy C.</au><au>Sun, Rifei</au><au>Walsh, John A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad‐spectrum virus resistance</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2014-01</date><risdate>2014</risdate><volume>77</volume><issue>2</issue><spage>261</spage><epage>268</epage><pages>261-268</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Recessive strain‐specific resistance to a number of plant viruses in the Potyvirus genus has been found to be based on mutations in the eukaryotic translation initiation factor 4E (eIF4E) and its isoform, eIF(iso)4E. We identified three copies of eIF(iso)4E in a number of Brassica rapa lines. Here we report broad‐spectrum resistance to the potyvirus Turnip mosaic virus (TuMV) due to a natural mechanism based on the mis‐splicing of the eIF(iso)4E allele in some TuMV‐resistant B. rapa var. pekinensis lines. Of the splice variants, the most common results in a stop codon in intron 1 and a much truncated, non‐functional protein. The existence of multiple copies has enabled redundancy in the host plant's translational machinery, resulting in diversification and emergence of the resistance. Deployment of the resistance is complicated by the presence of multiple copies of the gene. Our data suggest that in the B. rapa subspecies trilocularis, TuMV appears to be able to use copies of eIF(iso)4E at two loci. Transformation of different copies of eIF(iso)4E from a resistant B. rapa line into an eIF(iso)4E knockout line of Arabidopsis thaliana proved misleading because it showed that, when expressed ectopically, TuMV could use multiple copies which was not the case in the resistant B. rapa line. The inability of TuMV to access multiple copies of eIF(iso)4E in B. rapa and the broad spectrum of the resistance suggest it may be durable.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>24274163</pmid><doi>10.1111/tpj.12389</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis thaliana Brassica rapa Brassica rapa - genetics Brassica rapa - metabolism Brassica rapa - virology broad‐spectrum virus resistance Chinese cabbage Codon, Terminator eIF(iso)4E Eukaryotes Eukaryotic Initiation Factors - metabolism Genes, Plant Genes, Recessive Introns mis‐splicing Molecular Sequence Data Plant diseases Plant pathology Plant resistance Potyvirus Rape plants RNA Splicing Turnip mosaic virus |
title | Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad‐spectrum virus resistance |
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