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The Impact of Competition and Allelopathy on the Trade-Off between Plant Defense and Growth in Two Contrasting Tree Species

Identifieur interne : 000537 ( Pmc/Curation ); précédent : 000536; suivant : 000538

The Impact of Competition and Allelopathy on the Trade-Off between Plant Defense and Growth in Two Contrasting Tree Species

Auteurs : Catherine Fernandez [France] ; Yogan Monnier [France] ; Mathieu Santonja [France] ; Christiane Gallet [France] ; Leslie A. Weston [Australie] ; Bernard Prévosto [France] ; Amélie Saunier [France] ; Virginie Baldy [France] ; Anne Bousquet-Mélou [France]

Source :

RBID : PMC:4855863

Abstract

In contrast to plant-animal interactions, the conceptual framework regarding the impact of secondary metabolites in mediating plant-plant interference is currently less well defined. Here, we address hypotheses about the role of chemically-mediated plant-plant interference (i.e., allelopathy) as a driver of Mediterranean forest dynamics. Growth and defense abilities of a pioneer (Pinus halepensis) and a late-successional (Quercus pubescens) Mediterranean forest species were evaluated under three different plant interference conditions: (i) allelopathy simulated by application of aqueous needle extracts of Pinus, (ii) resource competition created by the physical presence of a neighboring species (Pinus or Quercus), and (iii) a combination of both allelopathy and competition. After 24 months of experimentation in simulated field conditions, Quercus was more affected by plant interference treatments than was Pinus, and a hierarchical response to biotic interference (allelopathy < competition < allelopathy + competition) was observed in terms of relative impact on growth and plant defense. Both species modulated their respective metabolic profiles according to plant interference treatment and thus their inherent chemical defense status, resulting in a physiological trade-off between plant growth and production of defense metabolites. For Quercus, an increase in secondary metabolite production and a decrease in plant growth were observed in all treatments. In contrast, this trade-off in Pinus was only observed in competition and allelopathy + competition treatments. Although Pinus and Quercus expressed differential responses when subjected to a single interference condition, either allelopathy or competition, species responses were similar or positively correlated when strong interference conditions (allelopathy + competition) were imposed.


Url:
DOI: 10.3389/fpls.2016.00594
PubMed: 27200062
PubMed Central: 4855863

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PMC:4855863

Le document en format XML

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<p>In contrast to plant-animal interactions, the conceptual framework regarding the impact of secondary metabolites in mediating plant-plant interference is currently less well defined. Here, we address hypotheses about the role of chemically-mediated plant-plant interference (i.e., allelopathy) as a driver of Mediterranean forest dynamics. Growth and defense abilities of a pioneer (
<italic>Pinus halepensis</italic>
) and a late-successional (
<italic>Quercus pubescens</italic>
) Mediterranean forest species were evaluated under three different plant interference conditions: (i) allelopathy simulated by application of aqueous needle extracts of
<italic>Pinus</italic>
, (ii) resource competition created by the physical presence of a neighboring species (
<italic>Pinus</italic>
or
<italic>Quercus</italic>
), and (iii) a combination of both allelopathy and competition. After 24 months of experimentation in simulated field conditions,
<italic>Quercus</italic>
was more affected by plant interference treatments than was
<italic>Pinus</italic>
, and a hierarchical response to biotic interference (allelopathy < competition < allelopathy + competition) was observed in terms of relative impact on growth and plant defense. Both species modulated their respective metabolic profiles according to plant interference treatment and thus their inherent chemical defense status, resulting in a physiological trade-off between plant growth and production of defense metabolites. For
<italic>Quercus</italic>
, an increase in secondary metabolite production and a decrease in plant growth were observed in all treatments. In contrast, this trade-off in
<italic>Pinus</italic>
was only observed in competition and allelopathy + competition treatments. Although
<italic>Pinus</italic>
and
<italic>Quercus</italic>
expressed differential responses when subjected to a single interference condition, either allelopathy or competition, species responses were similar or positively correlated when strong interference conditions (allelopathy + competition) were imposed.</p>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
<journal-title-group>
<journal-title>Frontiers in Plant Science</journal-title>
</journal-title-group>
<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27200062</article-id>
<article-id pub-id-type="pmc">4855863</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2016.00594</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>The Impact of Competition and Allelopathy on the Trade-Off between Plant Defense and Growth in Two Contrasting Tree Species</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Fernandez</surname>
<given-names>Catherine</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup></sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/307884/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Monnier</surname>
<given-names>Yogan</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup></sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/320197/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Santonja</surname>
<given-names>Mathieu</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/311534/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gallet</surname>
<given-names>Christiane</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/344705/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Weston</surname>
<given-names>Leslie A.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/311699/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Prévosto</surname>
<given-names>Bernard</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/344236/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Saunier</surname>
<given-names>Amélie</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/344233/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Baldy</surname>
<given-names>Virginie</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/311493/overview"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bousquet-Mélou</surname>
<given-names>Anne</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/320931/overview"></uri>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Institut Méditerranéen de Biodiversité et d'Ecologie Marine et Continentale - Aix Marseille Université - Centre National de la Recherche Scientifique - IRD - Avignon Université</institution>
<country>Marseille, France</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Laboratoire d'Ecologie Alpine - Université de Savoie-Mont-Blanc</institution>
<country>Chambéry, France</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Graham Centre for Agricultural Innovation- Charles Sturt University</institution>
<country>Wagga Wagga, NSW, Australia</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Institut National de Recherche en Sciences et Technologies Pour l'Environnement et l'Agriculture</institution>
<country>Aix-en-Provence, France</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Boris Rewald, University of Natural Resources and Life Sciences, Austria</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Monica Scognamiglio, Max Planck Institute for Chemical Ecology, Germany; Tara Joy Massad, Rhodes College, USA</p>
</fn>
<corresp id="fn001">*Correspondence: Catherine Fernandez
<email xlink:type="simple">catherine.fernandez@imbe.fr</email>
</corresp>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science</p>
</fn>
<fn fn-type="other" id="fn003">
<p>†These authors have contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>04</day>
<month>5</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>7</volume>
<elocation-id>594</elocation-id>
<history>
<date date-type="received">
<day>19</day>
<month>1</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>18</day>
<month>4</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2016 Fernandez, Monnier, Santonja, Gallet, Weston, Prévosto, Saunier, Baldy and Bousquet-Mélou.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Fernandez, Monnier, Santonja, Gallet, Weston, Prévosto, Saunier, Baldy and Bousquet-Mélou</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract>
<p>In contrast to plant-animal interactions, the conceptual framework regarding the impact of secondary metabolites in mediating plant-plant interference is currently less well defined. Here, we address hypotheses about the role of chemically-mediated plant-plant interference (i.e., allelopathy) as a driver of Mediterranean forest dynamics. Growth and defense abilities of a pioneer (
<italic>Pinus halepensis</italic>
) and a late-successional (
<italic>Quercus pubescens</italic>
) Mediterranean forest species were evaluated under three different plant interference conditions: (i) allelopathy simulated by application of aqueous needle extracts of
<italic>Pinus</italic>
, (ii) resource competition created by the physical presence of a neighboring species (
<italic>Pinus</italic>
or
<italic>Quercus</italic>
), and (iii) a combination of both allelopathy and competition. After 24 months of experimentation in simulated field conditions,
<italic>Quercus</italic>
was more affected by plant interference treatments than was
<italic>Pinus</italic>
, and a hierarchical response to biotic interference (allelopathy < competition < allelopathy + competition) was observed in terms of relative impact on growth and plant defense. Both species modulated their respective metabolic profiles according to plant interference treatment and thus their inherent chemical defense status, resulting in a physiological trade-off between plant growth and production of defense metabolites. For
<italic>Quercus</italic>
, an increase in secondary metabolite production and a decrease in plant growth were observed in all treatments. In contrast, this trade-off in
<italic>Pinus</italic>
was only observed in competition and allelopathy + competition treatments. Although
<italic>Pinus</italic>
and
<italic>Quercus</italic>
expressed differential responses when subjected to a single interference condition, either allelopathy or competition, species responses were similar or positively correlated when strong interference conditions (allelopathy + competition) were imposed.</p>
</abstract>
<kwd-group>
<kwd>allelopathy</kwd>
<kwd>competition</kwd>
<kwd>ecometabolomics</kwd>
<kwd>metabolic profiling</kwd>
<kwd>phenotypic response</kwd>
<kwd>
<italic>Pinus halepensis</italic>
</kwd>
<kwd>
<italic>Quercus pubescens</italic>
</kwd>
<kwd>secondary metabolism</kwd>
</kwd-group>
<funding-group>
<award-group>
<funding-source id="cn001">Agence Nationale de la Recherche
<named-content content-type="fundref-id">10.13039/501100001665</named-content>
</funding-source>
<award-id rid="cn001">ANR-12-BSV7-0016-01</award-id>
</award-group>
</funding-group>
<counts>
<fig-count count="7"></fig-count>
<table-count count="2"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="80"></ref-count>
<page-count count="14"></page-count>
<word-count count="9409"></word-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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