Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress
D satellite RNA (satRNA) is a strain of cucumber mosaic virus (CMV) satRNA that induces an epidemic lethal disease in tomato. No natural resistance or tolerance has ever been found. Previously, we demonstrated the involvement of programmed cell death in disease development. Here, transgenic tomato p...
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description | D satellite RNA (satRNA) is a strain of cucumber mosaic virus (CMV) satRNA that induces an epidemic lethal disease in tomato. No natural resistance or tolerance has ever been found. Previously, we demonstrated the involvement of programmed cell death in disease development. Here, transgenic tomato plants expressing animal antiapoptotic genes bcl-xL and ced-9 were generated through agrobacterium-mediated transformation. High expression of bcl-xL or ced-9 affected plant growth and seed development. Inoculation of seedlings with CMV/D satRNA at T1 and T2 generations resulted in delayed cell-death symptoms or absence of symptoms. The degree of symptom suppression was correlated with increasing expression levels of the transgenes. Survival rates were compared among inoculated transgenic lines expressing bcl-xL, ced-9, and bcl-xL (G138A), a loss-of-function mutant of bcl-xL. More than 80% of the bcl-xL and ced-9 T1 transgenic lines showed higher survival rates than the average for bcl-xL (G138A) transgenic lines. Total RNA extracted from surviving plants contained D satRNA, indicating systemic accumulation of D satRNA. Thus, expression of bcl-xL and ced-9 improved tolerance to, rather than resistance to, CMV/D satRNA infection. In addition, expression of bcl-xL and ced-9 specifically abrogated the formation of necrotic lesions, but not other symptoms, in tomato leaves during chilling at 4 degrees C. At 7 degrees C, temperature-induced leaf senescence was dramatically delayed in bcl-xL and ced-9 transgenic plants, and high levels of anthocyanins accumulated, possibly limiting oxidative stress. Hence, expression of these animal antiapoptotic genes improved plant survival under abiotic or biotic stress. |
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No natural resistance or tolerance has ever been found. Previously, we demonstrated the involvement of programmed cell death in disease development. Here, transgenic tomato plants expressing animal antiapoptotic genes bcl-xL and ced-9 were generated through agrobacterium-mediated transformation. High expression of bcl-xL or ced-9 affected plant growth and seed development. Inoculation of seedlings with CMV/D satRNA at T1 and T2 generations resulted in delayed cell-death symptoms or absence of symptoms. The degree of symptom suppression was correlated with increasing expression levels of the transgenes. Survival rates were compared among inoculated transgenic lines expressing bcl-xL, ced-9, and bcl-xL (G138A), a loss-of-function mutant of bcl-xL. More than 80% of the bcl-xL and ced-9 T1 transgenic lines showed higher survival rates than the average for bcl-xL (G138A) transgenic lines. Total RNA extracted from surviving plants contained D satRNA, indicating systemic accumulation of D satRNA. Thus, expression of bcl-xL and ced-9 improved tolerance to, rather than resistance to, CMV/D satRNA infection. In addition, expression of bcl-xL and ced-9 specifically abrogated the formation of necrotic lesions, but not other symptoms, in tomato leaves during chilling at 4 degrees C. At 7 degrees C, temperature-induced leaf senescence was dramatically delayed in bcl-xL and ced-9 transgenic plants, and high levels of anthocyanins accumulated, possibly limiting oxidative stress. Hence, expression of these animal antiapoptotic genes improved plant survival under abiotic or biotic stress.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0407094101</identifier><identifier>PMID: 15505199</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Abiotic stress ; Agrobacterium tumefaciens - genetics ; Animal cells ; Animals ; Apoptosis ; Apoptosis Regulatory Proteins ; Base Sequence ; bcl-X Protein ; bcl-xL gene ; Biological Sciences ; Caenorhabditis elegans Proteins - genetics ; ced-9 gene ; Cell death ; cold stress ; Cucumber mosaic virus ; Cucumber Mosaic Virus Satellite - genetics ; Cucumovirus - genetics ; Cucumovirus - pathogenicity ; disease resistance ; DNA, Viral - genetics ; Gene expression ; Genes ; Inoculation ; Leaves ; Lycopersicon esculentum ; Plant Diseases - genetics ; Plant Diseases - virology ; plant growth ; Plants ; Plants, Genetically Modified ; Proto-Oncogene Proteins - genetics ; Proto-Oncogene Proteins c-bcl-2 - genetics ; RNA ; satellite RNA ; Solanum lycopersicum - cytology ; Solanum lycopersicum - genetics ; Solanum lycopersicum - growth & development ; Solanum lycopersicum - virology ; Solanum lycopersicum var. lycopersicum ; Tomatoes ; Transformation, Genetic ; Transgenes ; Transgenic plants ; Viruses</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2004-11, Vol.101 (44), p.15805-15810</ispartof><rights>Copyright 1993/2004 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Nov 2, 2004</rights><rights>Copyright © 2004, The National Academy of Sciences 2004</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c550t-5f115e087f1baf32467ee7188c4b899d4676144038815ff6e197cc7a59772cc3</citedby><cites>FETCH-LOGICAL-c550t-5f115e087f1baf32467ee7188c4b899d4676144038815ff6e197cc7a59772cc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/101/44.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/3373718$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/3373718$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15505199$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xu, P</creatorcontrib><creatorcontrib>Rogers, S.J</creatorcontrib><creatorcontrib>Roossinck, M.J</creatorcontrib><title>Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>D satellite RNA (satRNA) is a strain of cucumber mosaic virus (CMV) satRNA that induces an epidemic lethal disease in tomato. No natural resistance or tolerance has ever been found. Previously, we demonstrated the involvement of programmed cell death in disease development. Here, transgenic tomato plants expressing animal antiapoptotic genes bcl-xL and ced-9 were generated through agrobacterium-mediated transformation. High expression of bcl-xL or ced-9 affected plant growth and seed development. Inoculation of seedlings with CMV/D satRNA at T1 and T2 generations resulted in delayed cell-death symptoms or absence of symptoms. The degree of symptom suppression was correlated with increasing expression levels of the transgenes. Survival rates were compared among inoculated transgenic lines expressing bcl-xL, ced-9, and bcl-xL (G138A), a loss-of-function mutant of bcl-xL. More than 80% of the bcl-xL and ced-9 T1 transgenic lines showed higher survival rates than the average for bcl-xL (G138A) transgenic lines. Total RNA extracted from surviving plants contained D satRNA, indicating systemic accumulation of D satRNA. Thus, expression of bcl-xL and ced-9 improved tolerance to, rather than resistance to, CMV/D satRNA infection. In addition, expression of bcl-xL and ced-9 specifically abrogated the formation of necrotic lesions, but not other symptoms, in tomato leaves during chilling at 4 degrees C. At 7 degrees C, temperature-induced leaf senescence was dramatically delayed in bcl-xL and ced-9 transgenic plants, and high levels of anthocyanins accumulated, possibly limiting oxidative stress. Hence, expression of these animal antiapoptotic genes improved plant survival under abiotic or biotic stress.</description><subject>Abiotic stress</subject><subject>Agrobacterium tumefaciens - genetics</subject><subject>Animal cells</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Apoptosis Regulatory Proteins</subject><subject>Base Sequence</subject><subject>bcl-X Protein</subject><subject>bcl-xL gene</subject><subject>Biological Sciences</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>ced-9 gene</subject><subject>Cell death</subject><subject>cold stress</subject><subject>Cucumber mosaic virus</subject><subject>Cucumber Mosaic Virus Satellite - genetics</subject><subject>Cucumovirus - genetics</subject><subject>Cucumovirus - pathogenicity</subject><subject>disease resistance</subject><subject>DNA, Viral - genetics</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Inoculation</subject><subject>Leaves</subject><subject>Lycopersicon esculentum</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - virology</subject><subject>plant growth</subject><subject>Plants</subject><subject>Plants, Genetically Modified</subject><subject>Proto-Oncogene Proteins - genetics</subject><subject>Proto-Oncogene Proteins c-bcl-2 - genetics</subject><subject>RNA</subject><subject>satellite RNA</subject><subject>Solanum lycopersicum - cytology</subject><subject>Solanum lycopersicum - genetics</subject><subject>Solanum lycopersicum - growth & development</subject><subject>Solanum lycopersicum - virology</subject><subject>Solanum lycopersicum var. lycopersicum</subject><subject>Tomatoes</subject><subject>Transformation, Genetic</subject><subject>Transgenes</subject><subject>Transgenic plants</subject><subject>Viruses</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk2PFCEQhjtG446jZy9GiQcTD71bNNDAwYPZrB_JJB5cz4Rm6FkmPdACvRkTf7z0zmRHveyBAKmnXqrqpapeYjjHwMnF6HU6BwocJMWAH1ULDBLXLZXwuFoANLwWtKFn1bOUtgAgmYCn1RlmDBiWclH9vtqP0abkgkehR9pnp8cw5pCdQRvrbUKdGer9qoTWyNh1LZHzKIedzgFZf6O9KUwOg43zsZzQrYt6qJ1fT4VH3poYkkt3Arpzd8opz48-r570ekj2xXFfVtefrq4vv9Srb5-_Xn5c1abUmWvWY8wsCN7jTvekoS23lmMhDO2ElOtybzGlQITArO9biyU3hmsmOW-MIcvqw0F2nLqdXRvrcylQjdHtdPylgnbq34h3N2oTbhVrqGCi5L875sfwc7Ipq51Lxg6D9jZMSbUcSEMwPAhizlsgdFZ8-x-4DVP0ZQaqAUwkmdeyujhA8_xStP19xRjU7L6a3Vcn90vG678bPfFHuwvw_gjMmSc5rCgtlACm-mkYst3nwqIH2IK8OiDblEO8ZwjhpNhTwm8O4V4HpTfRJfXj-9xf-YeilQ2QP3ie15I</recordid><startdate>20041102</startdate><enddate>20041102</enddate><creator>Xu, P</creator><creator>Rogers, S.J</creator><creator>Roossinck, M.J</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7QO</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20041102</creationdate><title>Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress</title><author>Xu, P ; Rogers, S.J ; Roossinck, M.J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c550t-5f115e087f1baf32467ee7188c4b899d4676144038815ff6e197cc7a59772cc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Abiotic stress</topic><topic>Agrobacterium tumefaciens - genetics</topic><topic>Animal cells</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Apoptosis Regulatory Proteins</topic><topic>Base Sequence</topic><topic>bcl-X Protein</topic><topic>bcl-xL gene</topic><topic>Biological Sciences</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>ced-9 gene</topic><topic>Cell death</topic><topic>cold stress</topic><topic>Cucumber mosaic virus</topic><topic>Cucumber Mosaic Virus Satellite - genetics</topic><topic>Cucumovirus - genetics</topic><topic>Cucumovirus - pathogenicity</topic><topic>disease resistance</topic><topic>DNA, Viral - genetics</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Inoculation</topic><topic>Leaves</topic><topic>Lycopersicon esculentum</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - virology</topic><topic>plant growth</topic><topic>Plants</topic><topic>Plants, Genetically Modified</topic><topic>Proto-Oncogene Proteins - genetics</topic><topic>Proto-Oncogene Proteins c-bcl-2 - genetics</topic><topic>RNA</topic><topic>satellite RNA</topic><topic>Solanum lycopersicum - cytology</topic><topic>Solanum lycopersicum - genetics</topic><topic>Solanum lycopersicum - growth & development</topic><topic>Solanum lycopersicum - virology</topic><topic>Solanum lycopersicum var. lycopersicum</topic><topic>Tomatoes</topic><topic>Transformation, Genetic</topic><topic>Transgenes</topic><topic>Transgenic plants</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xu, P</creatorcontrib><creatorcontrib>Rogers, S.J</creatorcontrib><creatorcontrib>Roossinck, M.J</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Biotechnology Research Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, P</au><au>Rogers, S.J</au><au>Roossinck, M.J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2004-11-02</date><risdate>2004</risdate><volume>101</volume><issue>44</issue><spage>15805</spage><epage>15810</epage><pages>15805-15810</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>D satellite RNA (satRNA) is a strain of cucumber mosaic virus (CMV) satRNA that induces an epidemic lethal disease in tomato. No natural resistance or tolerance has ever been found. Previously, we demonstrated the involvement of programmed cell death in disease development. Here, transgenic tomato plants expressing animal antiapoptotic genes bcl-xL and ced-9 were generated through agrobacterium-mediated transformation. High expression of bcl-xL or ced-9 affected plant growth and seed development. Inoculation of seedlings with CMV/D satRNA at T1 and T2 generations resulted in delayed cell-death symptoms or absence of symptoms. The degree of symptom suppression was correlated with increasing expression levels of the transgenes. Survival rates were compared among inoculated transgenic lines expressing bcl-xL, ced-9, and bcl-xL (G138A), a loss-of-function mutant of bcl-xL. More than 80% of the bcl-xL and ced-9 T1 transgenic lines showed higher survival rates than the average for bcl-xL (G138A) transgenic lines. Total RNA extracted from surviving plants contained D satRNA, indicating systemic accumulation of D satRNA. Thus, expression of bcl-xL and ced-9 improved tolerance to, rather than resistance to, CMV/D satRNA infection. In addition, expression of bcl-xL and ced-9 specifically abrogated the formation of necrotic lesions, but not other symptoms, in tomato leaves during chilling at 4 degrees C. At 7 degrees C, temperature-induced leaf senescence was dramatically delayed in bcl-xL and ced-9 transgenic plants, and high levels of anthocyanins accumulated, possibly limiting oxidative stress. Hence, expression of these animal antiapoptotic genes improved plant survival under abiotic or biotic stress.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>15505199</pmid><doi>10.1073/pnas.0407094101</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Abiotic stress Agrobacterium tumefaciens - genetics Animal cells Animals Apoptosis Apoptosis Regulatory Proteins Base Sequence bcl-X Protein bcl-xL gene Biological Sciences Caenorhabditis elegans Proteins - genetics ced-9 gene Cell death cold stress Cucumber mosaic virus Cucumber Mosaic Virus Satellite - genetics Cucumovirus - genetics Cucumovirus - pathogenicity disease resistance DNA, Viral - genetics Gene expression Genes Inoculation Leaves Lycopersicon esculentum Plant Diseases - genetics Plant Diseases - virology plant growth Plants Plants, Genetically Modified Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins c-bcl-2 - genetics RNA satellite RNA Solanum lycopersicum - cytology Solanum lycopersicum - genetics Solanum lycopersicum - growth & development Solanum lycopersicum - virology Solanum lycopersicum var. lycopersicum Tomatoes Transformation, Genetic Transgenes Transgenic plants Viruses |
title | Expression of antiapoptotic genes bcl-xL and ced-9 in tomato enhances tolerance to viral-induced necrosis and abiotic stress |
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