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Alternative Oxidase in Resistance to Biotic Stresses: Nicotiana attenuata AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not Manduca sexta Larvae1[W][OA]

Identifieur interne : 001093 ( Ncbi/Merge ); précédent : 001092; suivant : 001094

Alternative Oxidase in Resistance to Biotic Stresses: Nicotiana attenuata AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not Manduca sexta Larvae1[W][OA]

Auteurs : Lu Zhang ; Youngjoo Oh ; Hongyu Li ; Ian T. Baldwin ; Ivan Galis

Source :

RBID : PMC:3490609

Abstract

The role of the alternative respiratory pathway in the protection of plants against biotic stress was examined in transgenic tobacco (Nicotiana attenuata) plants (irAOX) silenced in the expression of ALTERNATIVE OXIDASE (AOX) gene. Wild-type and irAOX plants were independently challenged with (1) chewing herbivores (Manduca sexta), (2) piercing-sucking insects (Empoasca spp.), and (3) bacterial pathogens (Pseudomonas syringae pv tomato DC3000), showing that all these treatments can strongly elicit accumulation of AOX gene transcripts in wild-type plants. When N. attenuata chemical defenses and resistance were examined, irAOX plants showed wild-type levels of defense-related phytohormones, secondary metabolites, and resistance to M. sexta. In contrast, piercing-sucking leafhoppers (Empoasca spp.) caused more leaf damage and induced significantly higher salicylic acid levels in irAOX compared with wild-type plants in the field and/or glasshouse. Subsequently, irAOX plants accumulated lower levels of defense metabolites, 17-hydroxygeranyllinalool diterpene glycosides, caffeoylputrescine, and nicotine compared with wild-type plants under prolonged attack of Empoasca spp. in the glasshouse. Finally, an accelerated cell death phenotype was observed in irAOX plants infected with P. syringae, which correlated with higher levels of salicylic acid and hydrogen peroxide levels in pathogen-infected irAOX compared with wild-type leaves. Overall, the AOX-associated changes in phytohormone and/or redox levels appear to support the resistance of N. attenuata plants against cell piercing-sucking insects and modulate the progression of cell death in pathogen-infected tissues but are not effective against rapidly feeding specialist herbivore M. sexta.


Url:
DOI: 10.1104/pp.112.200865
PubMed: 22961128
PubMed Central: 3490609

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PMC:3490609

Le document en format XML

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<title xml:lang="en">Alternative Oxidase in Resistance to Biotic Stresses:
<italic>Nicotiana attenuata</italic>
AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not
<italic>Manduca sexta</italic>
Larvae
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[W]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[OA]</sup>
</xref>
</title>
<author>
<name sortKey="Zhang, Lu" sort="Zhang, Lu" uniqKey="Zhang L" first="Lu" last="Zhang">Lu Zhang</name>
</author>
<author>
<name sortKey="Oh, Youngjoo" sort="Oh, Youngjoo" uniqKey="Oh Y" first="Youngjoo" last="Oh">Youngjoo Oh</name>
</author>
<author>
<name sortKey="Li, Hongyu" sort="Li, Hongyu" uniqKey="Li H" first="Hongyu" last="Li">Hongyu Li</name>
</author>
<author>
<name sortKey="Baldwin, Ian T" sort="Baldwin, Ian T" uniqKey="Baldwin I" first="Ian T." last="Baldwin">Ian T. Baldwin</name>
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<author>
<name sortKey="Galis, Ivan" sort="Galis, Ivan" uniqKey="Galis I" first="Ivan" last="Galis">Ivan Galis</name>
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<title xml:lang="en" level="a" type="main">Alternative Oxidase in Resistance to Biotic Stresses:
<italic>Nicotiana attenuata</italic>
AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not
<italic>Manduca sexta</italic>
Larvae
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
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<sup>[W]</sup>
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<sup>[OA]</sup>
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<author>
<name sortKey="Zhang, Lu" sort="Zhang, Lu" uniqKey="Zhang L" first="Lu" last="Zhang">Lu Zhang</name>
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<author>
<name sortKey="Oh, Youngjoo" sort="Oh, Youngjoo" uniqKey="Oh Y" first="Youngjoo" last="Oh">Youngjoo Oh</name>
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<author>
<name sortKey="Li, Hongyu" sort="Li, Hongyu" uniqKey="Li H" first="Hongyu" last="Li">Hongyu Li</name>
</author>
<author>
<name sortKey="Baldwin, Ian T" sort="Baldwin, Ian T" uniqKey="Baldwin I" first="Ian T." last="Baldwin">Ian T. Baldwin</name>
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<name sortKey="Galis, Ivan" sort="Galis, Ivan" uniqKey="Galis I" first="Ivan" last="Galis">Ivan Galis</name>
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<series>
<title level="j">Plant Physiology</title>
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<div type="abstract" xml:lang="en">
<p>The role of the alternative respiratory pathway in the protection of plants against biotic stress was examined in transgenic tobacco (
<italic>Nicotiana attenuata</italic>
) plants (irAOX) silenced in the expression of
<italic>ALTERNATIVE OXIDASE</italic>
(
<italic>AOX</italic>
) gene. Wild-type and irAOX plants were independently challenged with (1) chewing herbivores (
<italic>Manduca sexta</italic>
), (2) piercing-sucking insects (
<italic>Empoasca</italic>
spp.), and (3) bacterial pathogens (
<italic>Pseudomonas syringae</italic>
pv
<italic>tomato</italic>
DC3000), showing that all these treatments can strongly elicit accumulation of
<italic>AOX</italic>
gene transcripts in wild-type plants. When
<italic>N. attenuata</italic>
chemical defenses and resistance were examined, irAOX plants showed wild-type levels of defense-related phytohormones, secondary metabolites, and resistance to
<italic>M. sexta</italic>
. In contrast, piercing-sucking leafhoppers (
<italic>Empoasca</italic>
spp.) caused more leaf damage and induced significantly higher salicylic acid levels in irAOX compared with wild-type plants in the field and/or glasshouse. Subsequently, irAOX plants accumulated lower levels of defense metabolites, 17-hydroxygeranyllinalool diterpene glycosides, caffeoylputrescine, and nicotine compared with wild-type plants under prolonged attack of
<italic>Empoasca</italic>
spp. in the glasshouse. Finally, an accelerated cell death phenotype was observed in irAOX plants infected with
<italic>P. syringae</italic>
, which correlated with higher levels of salicylic acid and hydrogen peroxide levels in pathogen-infected irAOX compared with wild-type leaves. Overall, the AOX-associated changes in phytohormone and/or redox levels appear to support the resistance of
<italic>N. attenuata</italic>
plants against cell piercing-sucking insects and modulate the progression of cell death in pathogen-infected tissues but are not effective against rapidly feeding specialist herbivore
<italic>M. sexta</italic>
.</p>
</div>
</front>
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<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Plant Physiol</journal-id>
<journal-id journal-id-type="iso-abbrev">Plant Physiol</journal-id>
<journal-id journal-id-type="hwp">plantphysiol</journal-id>
<journal-id journal-id-type="publisher-id">aspb</journal-id>
<journal-title-group>
<journal-title>Plant Physiology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0032-0889</issn>
<issn pub-type="epub">1532-2548</issn>
<publisher>
<publisher-name>American Society of Plant Biologists</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">22961128</article-id>
<article-id pub-id-type="pmc">3490609</article-id>
<article-id pub-id-type="publisher-id">200865</article-id>
<article-id pub-id-type="doi">10.1104/pp.112.200865</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plants Interacting with Other Organisms</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Alternative Oxidase in Resistance to Biotic Stresses:
<italic>Nicotiana attenuata</italic>
AOX Contributes to Resistance to a Pathogen and a Piercing-Sucking Insect But Not
<italic>Manduca sexta</italic>
Larvae
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[W]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[OA]</sup>
</xref>
</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Lu</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Oh</surname>
<given-names>Youngjoo</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Hongyu</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Baldwin</surname>
<given-names>Ian T.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Galis</surname>
<given-names>Ivan</given-names>
</name>
<xref ref-type="author-notes" rid="afn1">
<sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<aff id="aff1">Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena D-07745, Germany (L.Z., Y.O., I.T.B., I.G.); and School of Life Sciences, Lanzhou University, Lanzhou 730000, People’s Republic of China (L.Z., H.L.)</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<label>*</label>
Corresponding author; e-mail
<email>igalis@ice.mpg.de</email>
.</corresp>
<fn id="afn1" fn-type="present-address">
<label>2</label>
<p>Present address: Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan.</p>
</fn>
<fn>
<p>The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (
<ext-link ext-link-type="uri" xlink:href="http://www.plantphysiol.org">www.plantphysiol.org</ext-link>
) is: Ian T. Baldwin (
<email>baldwin@ice.mpg.de</email>
).</p>
</fn>
<fn id="fn1" fn-type="supported-by">
<label>1</label>
<p>This work was supported by the Max Planck Society.</p>
</fn>
<fn id="fn2">
<label>[W]</label>
<p>The online version of this article contains Web-only data.</p>
</fn>
<fn id="fn3">
<label>[OA]</label>
<p>Open Access articles can be viewed online without a subscription.</p>
</fn>
<fn>
<p>
<ext-link ext-link-type="uri" xlink:href="http://www.plantphysiol.org/cgi/doi/10.1104/pp.112.200865">www.plantphysiol.org/cgi/doi/10.1104/pp.112.200865</ext-link>
</p>
</fn>
</author-notes>
<pmc-comment>Fake ppub date generated by PMC from publisher pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub">
<month>11</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub">
<day>07</day>
<month>9</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>07</day>
<month>9</month>
<year>2012</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>160</volume>
<issue>3</issue>
<fpage>1453</fpage>
<lpage>1467</lpage>
<history>
<date date-type="received">
<day>22</day>
<month>5</month>
<year>2012</year>
</date>
<date date-type="accepted">
<day>03</day>
<month>9</month>
<year>2012</year>
</date>
</history>
<permissions>
<copyright-statement>© 2012 American Society of Plant Biologists. All Rights Reserved.</copyright-statement>
<copyright-year>2012</copyright-year>
</permissions>
<abstract>
<p>The role of the alternative respiratory pathway in the protection of plants against biotic stress was examined in transgenic tobacco (
<italic>Nicotiana attenuata</italic>
) plants (irAOX) silenced in the expression of
<italic>ALTERNATIVE OXIDASE</italic>
(
<italic>AOX</italic>
) gene. Wild-type and irAOX plants were independently challenged with (1) chewing herbivores (
<italic>Manduca sexta</italic>
), (2) piercing-sucking insects (
<italic>Empoasca</italic>
spp.), and (3) bacterial pathogens (
<italic>Pseudomonas syringae</italic>
pv
<italic>tomato</italic>
DC3000), showing that all these treatments can strongly elicit accumulation of
<italic>AOX</italic>
gene transcripts in wild-type plants. When
<italic>N. attenuata</italic>
chemical defenses and resistance were examined, irAOX plants showed wild-type levels of defense-related phytohormones, secondary metabolites, and resistance to
<italic>M. sexta</italic>
. In contrast, piercing-sucking leafhoppers (
<italic>Empoasca</italic>
spp.) caused more leaf damage and induced significantly higher salicylic acid levels in irAOX compared with wild-type plants in the field and/or glasshouse. Subsequently, irAOX plants accumulated lower levels of defense metabolites, 17-hydroxygeranyllinalool diterpene glycosides, caffeoylputrescine, and nicotine compared with wild-type plants under prolonged attack of
<italic>Empoasca</italic>
spp. in the glasshouse. Finally, an accelerated cell death phenotype was observed in irAOX plants infected with
<italic>P. syringae</italic>
, which correlated with higher levels of salicylic acid and hydrogen peroxide levels in pathogen-infected irAOX compared with wild-type leaves. Overall, the AOX-associated changes in phytohormone and/or redox levels appear to support the resistance of
<italic>N. attenuata</italic>
plants against cell piercing-sucking insects and modulate the progression of cell death in pathogen-infected tissues but are not effective against rapidly feeding specialist herbivore
<italic>M. sexta</italic>
.</p>
</abstract>
</article-meta>
<notes>
<glossary>
<title>Glossary</title>
<def-list>
<def-item>
<term id="term1">Cyt</term>
<def id="def1">
<p>cytochrome</p>
</def>
</def-item>
<def-item>
<term id="term2">UQ</term>
<def id="def2">
<p>ubiquinone</p>
</def>
</def-item>
<def-item>
<term id="term3">TMV</term>
<def id="def3">
<p>tobacco mosaic virus</p>
</def>
</def-item>
<def-item>
<term id="term4">PCD</term>
<def id="def4">
<p>programmed cell death</p>
</def>
</def-item>
<def-item>
<term id="term5">qRT-PCR</term>
<def id="def5">
<p>quantitative reverse transcription PCR</p>
</def>
</def-item>
<def-item>
<term id="term6">OS</term>
<def id="def6">
<p>oral secretions</p>
</def>
</def-item>
<def-item>
<term id="term7">RNAi</term>
<def id="def7">
<p>RNA interference</p>
</def>
</def-item>
<def-item>
<term id="term8">SA</term>
<def id="def8">
<p>salicylic acid</p>
</def>
</def-item>
<def-item>
<term id="term9">JA</term>
<def id="def9">
<p>jasmonic acid</p>
</def>
</def-item>
<def-item>
<term id="term10">
<italic>Pst</italic>
</term>
<def id="def10">
<p>
<italic>Pseudomonas syringae</italic>
pv
<italic>tomato</italic>
</p>
</def>
</def-item>
<def-item>
<term id="term11">DAB</term>
<def id="def11">
<p>3,3'-diaminobenzidine</p>
</def>
</def-item>
<def-item>
<term id="term12">HGL-DTG</term>
<def id="def12">
<p>17-hydroxygeranyllinalool diterpene glycoside</p>
</def>
</def-item>
<def-item>
<term id="term13">ROS</term>
<def id="def13">
<p>reactive oxygen species</p>
</def>
</def-item>
<def-item>
<term id="term14">CGA</term>
<def id="def14">
<p>chlorogenic acid</p>
</def>
</def-item>
<def-item>
<term id="term15">MRR</term>
<def id="def15">
<p>mitochondrial retrograde regulation</p>
</def>
</def-item>
<def-item>
<term id="term16">SHAM</term>
<def id="def16">
<p>salicylhydroxamic acid</p>
</def>
</def-item>
<def-item>
<term id="term17">SAR</term>
<def id="def17">
<p>systemic acquired resistance</p>
</def>
</def-item>
<def-item>
<term id="term18">cDNA</term>
<def id="def18">
<p>complementary DNA</p>
</def>
</def-item>
<def-item>
<term id="term19">CP</term>
<def id="def19">
<p>caffeoylputrescine</p>
</def>
</def-item>
<def-item>
<term id="term20">MeSA</term>
<def id="def20">
<p>methyl salicylic acid</p>
</def>
</def-item>
<def-item>
<term id="term21">H
<sub>2</sub>
O
<sub>2</sub>
</term>
<def id="def21">
<p>hydrogen peroxide</p>
</def>
</def-item>
</def-list>
</glossary>
</notes>
</front>
</pmc>
<affiliations>
<list></list>
<tree>
<noCountry>
<name sortKey="Baldwin, Ian T" sort="Baldwin, Ian T" uniqKey="Baldwin I" first="Ian T." last="Baldwin">Ian T. Baldwin</name>
<name sortKey="Galis, Ivan" sort="Galis, Ivan" uniqKey="Galis I" first="Ivan" last="Galis">Ivan Galis</name>
<name sortKey="Li, Hongyu" sort="Li, Hongyu" uniqKey="Li H" first="Hongyu" last="Li">Hongyu Li</name>
<name sortKey="Oh, Youngjoo" sort="Oh, Youngjoo" uniqKey="Oh Y" first="Youngjoo" last="Oh">Youngjoo Oh</name>
<name sortKey="Zhang, Lu" sort="Zhang, Lu" uniqKey="Zhang L" first="Lu" last="Zhang">Lu Zhang</name>
</noCountry>
</tree>
</affiliations>
</record>

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