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Terpene Down-Regulation in Orange Reveals the Role of Fruit Aromas in Mediating Interactions with Insect Herbivores and Pathogens1[C][W]

Identifieur interne : 000C92 ( Pmc/Corpus ); précédent : 000C91; suivant : 000C93

Terpene Down-Regulation in Orange Reveals the Role of Fruit Aromas in Mediating Interactions with Insect Herbivores and Pathogens1[C][W]

Auteurs : Ana Rodríguez ; Victoria San Andrés ; Magdalena Cervera ; Ana Redondo ; Berta Alquézar ; Takehiko Shimada ; José Gadea ; María Jesús Rodrigo ; Lorenzo Zacarías ; Lluís Palou ; María M. L Pez ; Pedro Casta Era ; Leandro Pe A

Source :

RBID : PMC:3177276

Abstract

Plants use volatile terpene compounds as odor cues for communicating with the environment. Fleshy fruits are particularly rich in volatiles that deter herbivores and attract seed dispersal agents. We have investigated how terpenes in citrus fruit peels affect the interaction between the plant, insects, and microorganisms. Because limonene represents up to 97% of the total volatiles in orange (Citrus sinensis) fruit peel, we chose to down-regulate the expression of a limonene synthase gene in orange plants by introducing an antisense construct of this gene. Transgenic fruits showed reduced accumulation of limonene in the peel. When these fruits were challenged with either the fungus Penicillium digitatum or with the bacterium Xanthomonas citri subsp. citri, they showed marked resistance against these pathogens that were unable to infect the peel tissues. Moreover, males of the citrus pest medfly (Ceratitis capitata) were less attracted to low limonene-expressing fruits than to control fruits. These results indicate that limonene accumulation in the peel of citrus fruit appears to be involved in the successful trophic interaction between fruits, insects, and microorganisms. Terpene down-regulation might be a strategy to generate broad-spectrum resistance against pests and pathogens in fleshy fruits from economically important crops. In addition, terpene engineering may be important for studying the basic ecological interactions between fruits, herbivores, and pathogens.


Url:
DOI: 10.1104/pp.111.176545
PubMed: 21525333
PubMed Central: 3177276

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PMC:3177276

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<p>Plants use volatile terpene compounds as odor cues for communicating with the environment. Fleshy fruits are particularly rich in volatiles that deter herbivores and attract seed dispersal agents. We have investigated how terpenes in citrus fruit peels affect the interaction between the plant, insects, and microorganisms. Because limonene represents up to 97% of the total volatiles in orange (
<italic>Citrus sinensis</italic>
) fruit peel, we chose to down-regulate the expression of a limonene synthase gene in orange plants by introducing an antisense construct of this gene. Transgenic fruits showed reduced accumulation of limonene in the peel. When these fruits were challenged with either the fungus
<italic>Penicillium digitatum</italic>
or with the bacterium
<italic>Xanthomonas citri</italic>
subsp.
<italic>citri</italic>
, they showed marked resistance against these pathogens that were unable to infect the peel tissues. Moreover, males of the citrus pest medfly (
<italic>Ceratitis capitata</italic>
) were less attracted to low limonene-expressing fruits than to control fruits. These results indicate that limonene accumulation in the peel of citrus fruit appears to be involved in the successful trophic interaction between fruits, insects, and microorganisms. Terpene down-regulation might be a strategy to generate broad-spectrum resistance against pests and pathogens in fleshy fruits from economically important crops. In addition, terpene engineering may be important for studying the basic ecological interactions between fruits, herbivores, and pathogens.</p>
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<subj-group subj-group-type="heading">
<subject>Plants Interacting with Other Organisms</subject>
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<title-group>
<article-title>Terpene Down-Regulation in Orange Reveals the Role of Fruit Aromas in Mediating Interactions with Insect Herbivores and Pathogens
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[W]</sup>
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<name>
<surname>Rodríguez</surname>
<given-names>Ana</given-names>
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<name>
<surname>San Andrés</surname>
<given-names>Victoria</given-names>
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<name>
<surname>Cervera</surname>
<given-names>Magdalena</given-names>
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<surname>Redondo</surname>
<given-names>Ana</given-names>
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<surname>Alquézar</surname>
<given-names>Berta</given-names>
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<contrib contrib-type="author">
<name>
<surname>Shimada</surname>
<given-names>Takehiko</given-names>
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<given-names>José</given-names>
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<name>
<surname>Rodrigo</surname>
<given-names>María Jesús</given-names>
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<name>
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<given-names>Lorenzo</given-names>
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<name>
<surname>Palou</surname>
<given-names>Lluís</given-names>
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<contrib contrib-type="author">
<name>
<surname>López</surname>
<given-names>María M.</given-names>
</name>
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<contrib contrib-type="author">
<name>
<surname>Castañera</surname>
<given-names>Pedro</given-names>
</name>
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<contrib contrib-type="author">
<name>
<surname>Peña</surname>
<given-names>Leandro</given-names>
</name>
<xref ref-type="corresp" rid="cor1">
<sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff>Centro de Protección Vegetal y Biotecnología (A.R., V.S.A., M.C., A.R., B.A., M.M.L., L. Peña) and Centro de Tecnología Postcosecha (L. Palou), Instituto Valenciano de Investigaciones Agrarias, 46113, Moncada, Valencia, Spain; Departamento Biología de Plantas, Centro de Investigaciones Biológicas-Consejo Superior de Investigaciones Científicas, 28040, Madrid, Spain (V.S.A., P.C.); Department of Citrus Research, National Institute of Fruit Tree Science, Tsukuba, Ibaraki 305–8605, Japan (T.S.); Homeostasis Iónica, Estrés Celular y Genómica, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.G.); Departamento de Ciencia de los Alimentos, Instituto de Agroquímica y Tecnología de Alimentos-Consejo Superior de Investigaciones Científicas, 46980, Paterna, Valencia, Spain (M.J.R., L.Z.)</aff>
<author-notes>
<corresp id="cor1">
<label>*</label>
Corresponding author; e-mail
<email>lpenya@ivia.es</email>
.</corresp>
<fn id="fn1">
<label>1</label>
<p>This work was supported by the Fondo Europeo de Desarrollo Regional and the Ministry of Science and Innovation of Spain (grant no. AGL2009–08052). A.R. was supported by a Ph.D. fellowship from the Instituto Valenciano de Investigaciones Agrarias, Spain.</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="www.plantphysiol.org">www.plantphysiol.org</ext-link>
) is: Leandro Peña (
<email>lpenya@ivia.es</email>
).</p>
</fn>
<fn id="fn2">
<label>[C]</label>
<p>Some figures in this article are displayed in color online but in black and white in the print edition.</p>
</fn>
<fn id="fn3">
<label>[W]</label>
<p>The online version of this article contains Web-only data.</p>
</fn>
<fn>
<p>
<ext-link ext-link-type="uri" xlink:href="www.plantphysiol.org/cgi/doi/10.1104/pp.111.176545">www.plantphysiol.org/cgi/doi/10.1104/pp.111.176545</ext-link>
</p>
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<pmc-comment>Fake ppub date generated by PMC from publisher pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub">
<month>6</month>
<year>2011</year>
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<pub-date pub-type="epub">
<day>27</day>
<month>4</month>
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<volume>156</volume>
<issue>2</issue>
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<lpage>802</lpage>
<history>
<date date-type="received">
<day>16</day>
<month>3</month>
<year>2011</year>
</date>
<date date-type="accepted">
<day>26</day>
<month>4</month>
<year>2011</year>
</date>
</history>
<permissions>
<copyright-statement>© 2011 American Society of Plant Biologists</copyright-statement>
<copyright-year>2011</copyright-year>
</permissions>
<abstract>
<p>Plants use volatile terpene compounds as odor cues for communicating with the environment. Fleshy fruits are particularly rich in volatiles that deter herbivores and attract seed dispersal agents. We have investigated how terpenes in citrus fruit peels affect the interaction between the plant, insects, and microorganisms. Because limonene represents up to 97% of the total volatiles in orange (
<italic>Citrus sinensis</italic>
) fruit peel, we chose to down-regulate the expression of a limonene synthase gene in orange plants by introducing an antisense construct of this gene. Transgenic fruits showed reduced accumulation of limonene in the peel. When these fruits were challenged with either the fungus
<italic>Penicillium digitatum</italic>
or with the bacterium
<italic>Xanthomonas citri</italic>
subsp.
<italic>citri</italic>
, they showed marked resistance against these pathogens that were unable to infect the peel tissues. Moreover, males of the citrus pest medfly (
<italic>Ceratitis capitata</italic>
) were less attracted to low limonene-expressing fruits than to control fruits. These results indicate that limonene accumulation in the peel of citrus fruit appears to be involved in the successful trophic interaction between fruits, insects, and microorganisms. Terpene down-regulation might be a strategy to generate broad-spectrum resistance against pests and pathogens in fleshy fruits from economically important crops. In addition, terpene engineering may be important for studying the basic ecological interactions between fruits, herbivores, and pathogens.</p>
</abstract>
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</front>
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