Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus
Salicylic acid (SA), a natural defensive signal chemical, and antimycin A, a cytochrome pathway inhibitor, induce resistance to Tobacco mosaic virus (TMV). Pharmacological evidence suggested signaling during resistance induction by both chemicals involved alternative oxidase (AOX), sole component of...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2003-07, Vol.132 (3), p.1518-1528 |
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| creator | Gilliland, A Singh, D.P Hayward, J.M Moore, C.A Murphy, A.M York, C.J Slator, J Carr, J.P |
| description | Salicylic acid (SA), a natural defensive signal chemical, and antimycin A, a cytochrome pathway inhibitor, induce resistance to Tobacco mosaic virus (TMV). Pharmacological evidence suggested signaling during resistance induction by both chemicals involved alternative oxidase (AOX), sole component of the alternative respiratory pathway (AP). Roles of the AP include regulation of intramitochondrial reactive oxygen species and maintenance of metabolic homeostasis. Transgenic tobacco (Nicotiana tabacum) with modified AP capacities (2- to 3-fold increased or decreased) showed no alteration in phenotype with respect to basal susceptibility to TMV or the ability to display SA-induced resistance to systemic viral disease. However, in directly inoculated tissue, antimycin A-induced TMV resistance was inhibited in plants with increased AP capacities, whereas SA and antimycin A-induced resistance was transiently enhanced in plant lines with decreased AP capacities. We conclude that SA-induced TMV resistance results from activation of multiple mechanisms, a subset of which are inducible by antimycin A and influenced by AOX. Other antiviral factors, potentially including the SA-inducible RNA-dependent RNA polymerase, are regulated by AOX-independent mechanisms. |
| doi_str_mv | 10.1104/pp.102.017640 |
| format | Article |
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Pharmacological evidence suggested signaling during resistance induction by both chemicals involved alternative oxidase (AOX), sole component of the alternative respiratory pathway (AP). Roles of the AP include regulation of intramitochondrial reactive oxygen species and maintenance of metabolic homeostasis. Transgenic tobacco (Nicotiana tabacum) with modified AP capacities (2- to 3-fold increased or decreased) showed no alteration in phenotype with respect to basal susceptibility to TMV or the ability to display SA-induced resistance to systemic viral disease. However, in directly inoculated tissue, antimycin A-induced TMV resistance was inhibited in plants with increased AP capacities, whereas SA and antimycin A-induced resistance was transiently enhanced in plant lines with decreased AP capacities. We conclude that SA-induced TMV resistance results from activation of multiple mechanisms, a subset of which are inducible by antimycin A and influenced by AOX. Other antiviral factors, potentially including the SA-inducible RNA-dependent RNA polymerase, are regulated by AOX-independent mechanisms.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.102.017640</identifier><identifier>PMID: 12857832</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Agronomy. Soil science and plant productions ; alternative oxidase ; alternative respiration ; antimycin A ; Antimycin A - pharmacology ; biochemical pathways ; Biological and medical sciences ; Cell Respiration - drug effects ; Cell Respiration - genetics ; cytochromes ; disease resistance ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Gene expression regulation ; Genetics and breeding of economic plants ; Inoculation ; Leaves ; Mitochondria ; Mitochondrial Proteins ; Nicotiana - drug effects ; Nicotiana - genetics ; Nicotiana - metabolism ; Nicotiana - virology ; Nicotiana tabacum ; Oxidases ; oxidoreductases ; Oxidoreductases - genetics ; Oxidoreductases - metabolism ; Pest resistance ; Phenotype ; Plant Diseases - genetics ; Plant Diseases - virology ; Plant Leaves - drug effects ; Plant Leaves - genetics ; Plant Leaves - metabolism ; Plant pathogens ; Plant Proteins ; plant viruses ; Plants ; Plants Interacting with Other Organisms ; Plants, Genetically Modified ; Reactive oxygen species ; resistance mechanisms ; RNA-directed RNA polymerase ; salicylic acid ; Salicylic Acid - pharmacology ; signal transduction ; Tobacco mosaic virus ; Tobacco Mosaic Virus - drug effects ; Tobacco Mosaic Virus - enzymology ; Tobacco Mosaic Virus - metabolism ; transgenes ; Transgenic plants ; Varietal selection. Specialized plant breeding, plant breeding aims ; Viruses</subject><ispartof>Plant physiology (Bethesda), 2003-07, Vol.132 (3), p.1518-1528</ispartof><rights>Copyright 2003 American Society of Plant Biologists</rights><rights>2003 INIST-CNRS</rights><rights>Copyright © 2003, The American Society for Plant Biologists 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c591t-4f35622d0f737fb515e3970bcdeb1f0e6c8fd2186b3cadff6e25f85b8ac9e74d3</citedby><cites>FETCH-LOGICAL-c591t-4f35622d0f737fb515e3970bcdeb1f0e6c8fd2186b3cadff6e25f85b8ac9e74d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4281230$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4281230$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27903,27904,57995,58228</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=14951404$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12857832$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gilliland, A</creatorcontrib><creatorcontrib>Singh, D.P</creatorcontrib><creatorcontrib>Hayward, J.M</creatorcontrib><creatorcontrib>Moore, C.A</creatorcontrib><creatorcontrib>Murphy, A.M</creatorcontrib><creatorcontrib>York, C.J</creatorcontrib><creatorcontrib>Slator, J</creatorcontrib><creatorcontrib>Carr, J.P</creatorcontrib><title>Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Salicylic acid (SA), a natural defensive signal chemical, and antimycin A, a cytochrome pathway inhibitor, induce resistance to Tobacco mosaic virus (TMV). Pharmacological evidence suggested signaling during resistance induction by both chemicals involved alternative oxidase (AOX), sole component of the alternative respiratory pathway (AP). Roles of the AP include regulation of intramitochondrial reactive oxygen species and maintenance of metabolic homeostasis. Transgenic tobacco (Nicotiana tabacum) with modified AP capacities (2- to 3-fold increased or decreased) showed no alteration in phenotype with respect to basal susceptibility to TMV or the ability to display SA-induced resistance to systemic viral disease. However, in directly inoculated tissue, antimycin A-induced TMV resistance was inhibited in plants with increased AP capacities, whereas SA and antimycin A-induced resistance was transiently enhanced in plant lines with decreased AP capacities. We conclude that SA-induced TMV resistance results from activation of multiple mechanisms, a subset of which are inducible by antimycin A and influenced by AOX. Other antiviral factors, potentially including the SA-inducible RNA-dependent RNA polymerase, are regulated by AOX-independent mechanisms.</description><subject>Agronomy. Soil science and plant productions</subject><subject>alternative oxidase</subject><subject>alternative respiration</subject><subject>antimycin A</subject><subject>Antimycin A - pharmacology</subject><subject>biochemical pathways</subject><subject>Biological and medical sciences</subject><subject>Cell Respiration - drug effects</subject><subject>Cell Respiration - genetics</subject><subject>cytochromes</subject><subject>disease resistance</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Gene expression regulation</subject><subject>Genetics and breeding of economic plants</subject><subject>Inoculation</subject><subject>Leaves</subject><subject>Mitochondria</subject><subject>Mitochondrial Proteins</subject><subject>Nicotiana - drug effects</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - metabolism</subject><subject>Nicotiana - virology</subject><subject>Nicotiana tabacum</subject><subject>Oxidases</subject><subject>oxidoreductases</subject><subject>Oxidoreductases - genetics</subject><subject>Oxidoreductases - metabolism</subject><subject>Pest resistance</subject><subject>Phenotype</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - virology</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - metabolism</subject><subject>Plant pathogens</subject><subject>Plant Proteins</subject><subject>plant viruses</subject><subject>Plants</subject><subject>Plants Interacting with Other Organisms</subject><subject>Plants, Genetically Modified</subject><subject>Reactive oxygen species</subject><subject>resistance mechanisms</subject><subject>RNA-directed RNA polymerase</subject><subject>salicylic acid</subject><subject>Salicylic Acid - pharmacology</subject><subject>signal transduction</subject><subject>Tobacco mosaic virus</subject><subject>Tobacco Mosaic Virus - drug effects</subject><subject>Tobacco Mosaic Virus - enzymology</subject><subject>Tobacco Mosaic Virus - metabolism</subject><subject>transgenes</subject><subject>Transgenic plants</subject><subject>Varietal selection. Specialized plant breeding, plant breeding aims</subject><subject>Viruses</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhiMEokvhyA2BL_SWxZ-Jc-ihqqBFqsSB9mw5zrh1lcTBTlbaf8NPZaqstnDiYHns95nx2K-L4j2jW8ao_DJNW0b5lrK6kvRFsWFK8JIrqV8WG0oxplo3J8WbnB8ppUww-bo4YVyrWgu-KX5fwQhzcGSIXfDB2TnEkURPbD9DGnG5A5IgTyGt0oPNBEkPCcY52J4Axm7OBDWLO8PehZFclGHsFgcd2UHKSybZ9sHtcRDrQndUsXLIsx0dkDmS29ha5yL2ki2Su5CW_LZ45W2f4d1hPi3uvn29vbwub35cfb-8uCmdathcSi9UxXlHfS1q3yqmQDQ1bV0HLfMUKqd9x5muWuFs530FXHmtWm1dA7XsxGlxvtadlnaAzuHtku3NlMJg095EG8y_yhgezH3cGVbVtKGYf3bIT_HXAnk2Q8gO-t6OEJdsaiFVI1jzX5DVaBjjCsFyBV2KOSfwx2YYNU_em2nCkJvVe-Q__n2DZ_pgNgKfD4DNzvY-4buH_MzJRjFJJXIfVu4xzzEddck14-LpnE-r7G009j5hibufHL8WZVRTLhvxB6Jpz7o</recordid><startdate>20030701</startdate><enddate>20030701</enddate><creator>Gilliland, A</creator><creator>Singh, D.P</creator><creator>Hayward, J.M</creator><creator>Moore, C.A</creator><creator>Murphy, A.M</creator><creator>York, C.J</creator><creator>Slator, J</creator><creator>Carr, J.P</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Physiologists</general><general>The American Society for Plant Biologists</general><scope>FBQ</scope><scope>IQODW</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>7T7</scope><scope>7TM</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20030701</creationdate><title>Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus</title><author>Gilliland, A ; Singh, D.P ; Hayward, J.M ; Moore, C.A ; Murphy, A.M ; York, C.J ; Slator, J ; Carr, J.P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c591t-4f35622d0f737fb515e3970bcdeb1f0e6c8fd2186b3cadff6e25f85b8ac9e74d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Agronomy. Soil science and plant productions</topic><topic>alternative oxidase</topic><topic>alternative respiration</topic><topic>antimycin A</topic><topic>Antimycin A - pharmacology</topic><topic>biochemical pathways</topic><topic>Biological and medical sciences</topic><topic>Cell Respiration - drug effects</topic><topic>Cell Respiration - genetics</topic><topic>cytochromes</topic><topic>disease resistance</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene expression</topic><topic>Gene expression regulation</topic><topic>Genetics and breeding of economic plants</topic><topic>Inoculation</topic><topic>Leaves</topic><topic>Mitochondria</topic><topic>Mitochondrial Proteins</topic><topic>Nicotiana - drug effects</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - metabolism</topic><topic>Nicotiana - virology</topic><topic>Nicotiana tabacum</topic><topic>Oxidases</topic><topic>oxidoreductases</topic><topic>Oxidoreductases - genetics</topic><topic>Oxidoreductases - metabolism</topic><topic>Pest resistance</topic><topic>Phenotype</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - virology</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - metabolism</topic><topic>Plant pathogens</topic><topic>Plant Proteins</topic><topic>plant viruses</topic><topic>Plants</topic><topic>Plants Interacting with Other Organisms</topic><topic>Plants, Genetically Modified</topic><topic>Reactive oxygen species</topic><topic>resistance mechanisms</topic><topic>RNA-directed RNA polymerase</topic><topic>salicylic acid</topic><topic>Salicylic Acid - pharmacology</topic><topic>signal transduction</topic><topic>Tobacco mosaic virus</topic><topic>Tobacco Mosaic Virus - drug effects</topic><topic>Tobacco Mosaic Virus - enzymology</topic><topic>Tobacco Mosaic Virus - metabolism</topic><topic>transgenes</topic><topic>Transgenic plants</topic><topic>Varietal selection. Specialized plant breeding, plant breeding aims</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gilliland, A</creatorcontrib><creatorcontrib>Singh, D.P</creatorcontrib><creatorcontrib>Hayward, J.M</creatorcontrib><creatorcontrib>Moore, C.A</creatorcontrib><creatorcontrib>Murphy, A.M</creatorcontrib><creatorcontrib>York, C.J</creatorcontrib><creatorcontrib>Slator, J</creatorcontrib><creatorcontrib>Carr, J.P</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gilliland, A</au><au>Singh, D.P</au><au>Hayward, J.M</au><au>Moore, C.A</au><au>Murphy, A.M</au><au>York, C.J</au><au>Slator, J</au><au>Carr, J.P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2003-07-01</date><risdate>2003</risdate><volume>132</volume><issue>3</issue><spage>1518</spage><epage>1528</epage><pages>1518-1528</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Salicylic acid (SA), a natural defensive signal chemical, and antimycin A, a cytochrome pathway inhibitor, induce resistance to Tobacco mosaic virus (TMV). Pharmacological evidence suggested signaling during resistance induction by both chemicals involved alternative oxidase (AOX), sole component of the alternative respiratory pathway (AP). Roles of the AP include regulation of intramitochondrial reactive oxygen species and maintenance of metabolic homeostasis. Transgenic tobacco (Nicotiana tabacum) with modified AP capacities (2- to 3-fold increased or decreased) showed no alteration in phenotype with respect to basal susceptibility to TMV or the ability to display SA-induced resistance to systemic viral disease. However, in directly inoculated tissue, antimycin A-induced TMV resistance was inhibited in plants with increased AP capacities, whereas SA and antimycin A-induced resistance was transiently enhanced in plant lines with decreased AP capacities. We conclude that SA-induced TMV resistance results from activation of multiple mechanisms, a subset of which are inducible by antimycin A and influenced by AOX. Other antiviral factors, potentially including the SA-inducible RNA-dependent RNA polymerase, are regulated by AOX-independent mechanisms.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>12857832</pmid><doi>10.1104/pp.102.017640</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Agronomy. Soil science and plant productions alternative oxidase alternative respiration antimycin A Antimycin A - pharmacology biochemical pathways Biological and medical sciences Cell Respiration - drug effects Cell Respiration - genetics cytochromes disease resistance Fundamental and applied biological sciences. Psychology Gene expression Gene expression regulation Genetics and breeding of economic plants Inoculation Leaves Mitochondria Mitochondrial Proteins Nicotiana - drug effects Nicotiana - genetics Nicotiana - metabolism Nicotiana - virology Nicotiana tabacum Oxidases oxidoreductases Oxidoreductases - genetics Oxidoreductases - metabolism Pest resistance Phenotype Plant Diseases - genetics Plant Diseases - virology Plant Leaves - drug effects Plant Leaves - genetics Plant Leaves - metabolism Plant pathogens Plant Proteins plant viruses Plants Plants Interacting with Other Organisms Plants, Genetically Modified Reactive oxygen species resistance mechanisms RNA-directed RNA polymerase salicylic acid Salicylic Acid - pharmacology signal transduction Tobacco mosaic virus Tobacco Mosaic Virus - drug effects Tobacco Mosaic Virus - enzymology Tobacco Mosaic Virus - metabolism transgenes Transgenic plants Varietal selection. Specialized plant breeding, plant breeding aims Viruses |
| title | Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus |
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