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Temporal interactions of plant - insect - predator after infection of bacterial pathogen on rice plants

Identifieur interne : 000088 ( Pmc/Curation ); précédent : 000087; suivant : 000089

Temporal interactions of plant - insect - predator after infection of bacterial pathogen on rice plants

Auteurs : Ze Sun [République populaire de Chine] ; Zhuang Liu [République populaire de Chine] ; Wen Zhou [République populaire de Chine] ; Huanan Jin [République populaire de Chine] ; Hao Liu [République populaire de Chine] ; Aiming Zhou [République populaire de Chine] ; Aijun Zhang [États-Unis] ; Man-Qun Wang [République populaire de Chine]

Source :

RBID : PMC:4868983

Abstract

Pathogenic infection on plants may affect interactions of host-plants with their herbivores, as well as the herbivores with their predators. In this study, the effects of infection by pathogenic bacterium Xanthomonas oryzae pv. oryzae (Xoo), which causes a vascular disease in rice, on rice plants and consequent interactions with a rice herbivore, brown rice planthopper (BPH) Nilaparvata lugens, and its major predator, Cyrtorhinus lividipennis, were investigated. The results showed that the rice plants exhibited increased resistance to BPH only at 3 d post-inoculation of Xoo, while the Xoo infection did not affect the development and fecundity of BPH. BPH exhibited a higher preference to Xoo infected rice plants, whereas C. lividipennis preferred the Xoo infected rice plants after BPH fed, but preferred healthy rice plants without BPH fed. Volatile organic compounds emitted from Xoo rice were significantly higher than those from healthy rice plants, Xoo infection on BPH fed plants caused rice plants to emit more the herbivore-induced plant volatiles, while all of these changes correlated to the temporal dimension. These results demonstrated that Xoo infection significantly influenced the interactions of rice plants with two non-vectors, BPH and its predator, although these effects exhibited in a temporal pattern after infection.


Url:
DOI: 10.1038/srep26043
PubMed: 27185548
PubMed Central: 4868983

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PMC:4868983

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<p>Pathogenic infection on plants may affect interactions of host-plants with their herbivores, as well as the herbivores with their predators. In this study, the effects of infection by pathogenic bacterium
<italic>Xanthomonas oryzae</italic>
pv.
<italic>oryzae</italic>
(
<italic>Xoo</italic>
), which causes a vascular disease in rice, on rice plants and consequent interactions with a rice herbivore, brown rice planthopper (BPH)
<italic>Nilaparvata lugens</italic>
, and its major predator,
<italic>Cyrtorhinus lividipennis</italic>
, were investigated. The results showed that the rice plants exhibited increased resistance to BPH only at 3 d post-inoculation of
<italic>Xoo</italic>
, while the
<italic>Xoo</italic>
infection did not affect the development and fecundity of BPH. BPH exhibited a higher preference to
<italic>Xoo</italic>
infected rice plants, whereas
<italic>C. lividipennis</italic>
preferred the
<italic>Xoo</italic>
infected rice plants after BPH fed, but preferred healthy rice plants without BPH fed. Volatile organic compounds emitted from
<italic>Xoo</italic>
rice were significantly higher than those from healthy rice plants,
<italic>Xoo</italic>
infection on BPH fed plants caused rice plants to emit more the herbivore-induced plant volatiles, while all of these changes correlated to the temporal dimension. These results demonstrated that
<italic>Xoo</italic>
infection significantly influenced the interactions of rice plants with two non-vectors, BPH and its predator, although these effects exhibited in a temporal pattern after infection.</p>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group>
<journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher>
<publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27185548</article-id>
<article-id pub-id-type="pmc">4868983</article-id>
<article-id pub-id-type="pii">srep26043</article-id>
<article-id pub-id-type="doi">10.1038/srep26043</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Temporal interactions of plant - insect - predator after infection of bacterial pathogen on rice plants</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Sun</surname>
<given-names>Ze</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="author-notes" rid="n1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Liu</surname>
<given-names>Zhuang</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="author-notes" rid="n1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhou</surname>
<given-names>Wen</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jin</surname>
<given-names>Huanan</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Liu</surname>
<given-names>Hao</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhou</surname>
<given-names>Aiming</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Aijun</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Man-Qun</given-names>
</name>
<xref ref-type="corresp" rid="c1">a</xref>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<aff id="a1">
<label>1</label>
<institution>Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University</institution>
, Wuhan 430070,
<country>P. R. China</country>
</aff>
<aff id="a2">
<label>2</label>
<institution>Invasive Insect Biocontrol and Behavior Laboratory, BARC-West, USDA-ARS</institution>
, Beltsville, MD 20705-2350,
<country>USA</country>
.</aff>
</contrib-group>
<author-notes>
<corresp id="c1">
<label>a</label>
<email>mqwang@mail.hzau.edu.cn</email>
</corresp>
<fn id="n1">
<label>*</label>
<p>These authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>17</day>
<month>05</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>6</volume>
<elocation-id>26043</elocation-id>
<history>
<date date-type="received">
<day>10</day>
<month>02</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>26</day>
<month>04</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2016, Macmillan Publishers Limited</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Macmillan Publishers Limited</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/">
<pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract>
<p>Pathogenic infection on plants may affect interactions of host-plants with their herbivores, as well as the herbivores with their predators. In this study, the effects of infection by pathogenic bacterium
<italic>Xanthomonas oryzae</italic>
pv.
<italic>oryzae</italic>
(
<italic>Xoo</italic>
), which causes a vascular disease in rice, on rice plants and consequent interactions with a rice herbivore, brown rice planthopper (BPH)
<italic>Nilaparvata lugens</italic>
, and its major predator,
<italic>Cyrtorhinus lividipennis</italic>
, were investigated. The results showed that the rice plants exhibited increased resistance to BPH only at 3 d post-inoculation of
<italic>Xoo</italic>
, while the
<italic>Xoo</italic>
infection did not affect the development and fecundity of BPH. BPH exhibited a higher preference to
<italic>Xoo</italic>
infected rice plants, whereas
<italic>C. lividipennis</italic>
preferred the
<italic>Xoo</italic>
infected rice plants after BPH fed, but preferred healthy rice plants without BPH fed. Volatile organic compounds emitted from
<italic>Xoo</italic>
rice were significantly higher than those from healthy rice plants,
<italic>Xoo</italic>
infection on BPH fed plants caused rice plants to emit more the herbivore-induced plant volatiles, while all of these changes correlated to the temporal dimension. These results demonstrated that
<italic>Xoo</italic>
infection significantly influenced the interactions of rice plants with two non-vectors, BPH and its predator, although these effects exhibited in a temporal pattern after infection.</p>
</abstract>
</article-meta>
</front>
<floats-group>
<fig id="f1">
<label>Figure 1</label>
<caption>
<title>BPH activities as identified by electrical penetration graph (EPG) recordings within the first 12 h at 1 to 6 days after
<italic>Xoo</italic>
infestation (mean ± SE, n = 9–15).</title>
<p>PI: plants infected by
<italic>Xoo</italic>
. (
<bold>a</bold>
) Time interval to the 1st N4a. (
<bold>b</bold>
) Total duration of N4b. (
<bold>c</bold>
) Total duration of np. (
<bold>d</bold>
) Total duration of ph. (
<bold>e</bold>
) Total number of ph. Waveform: np (non-penetration), ph (path way waveform), N4a (Sieve element salivation), N4b (ingestion in phloem). Asterisks show significant differences from the control group (*
<italic>p</italic>
 < 0.05; **
<italic>p</italic>
 < 0.01).</p>
</caption>
<graphic xlink:href="srep26043-f1"></graphic>
</fig>
<fig id="f2">
<label>Figure 2</label>
<caption>
<title>BPH activities as identified by electrical penetration graph (EPG) recordings within the first 12 h at 10 and 15 days after
<italic>Xoo</italic>
infestation (mean ± SE, n = 9–15).</title>
<p>PI: plants infected by
<italic>Xoo</italic>
. (
<bold>a</bold>
) Time interval to 1st N4a. (
<bold>b</bold>
) Total duration of N4b. (
<bold>c</bold>
) Total duration of np. (
<bold>d</bold>
) Total duration of ph. (
<bold>e</bold>
) Total number of ph. Waveform: np (non-penetration), ph (path way waveform), N4a (sieve element salivation), N4b (ingestion in phloem).</p>
</caption>
<graphic xlink:href="srep26043-f2"></graphic>
</fig>
<fig id="f3">
<label>Figure 3</label>
<caption>
<title>The duration (mean ± SE, n = 5) of BPH nymph of 3th instar, 4th instar, 5th instar and the total duration from 3th instar to newly emerged adult on healthy and infected rice plants.</title>
<p>PI: plants infected by
<italic>Xoo</italic>
for 5 days.</p>
</caption>
<graphic xlink:href="srep26043-f3"></graphic>
</fig>
<fig id="f4">
<label>Figure 4</label>
<caption>
<title>The number (mean ± SE, n = 7–8) of female BPH adults in two-choice assays between healthy rice plants and rice infected by
<italic>Xoo</italic>
in semi-natural foraging experiments.</title>
<p>PI: plants infected by
<italic>Xoo</italic>
. (
<bold>a–d</bold>
) the number of the BPH on plants at 3, 5, 10, 15 days after treatment with (dark line) or without (orange line)
<italic>Xoo</italic>
. Asterisks show significant differences among the treatments (*
<italic>p</italic>
 < 0.05).</p>
</caption>
<graphic xlink:href="srep26043-f4"></graphic>
</fig>
<fig id="f5">
<label>Figure 5</label>
<caption>
<title>The number of BPH and
<italic>C. lividipennis</italic>
attracted by volatiles released from the different rice treatments.</title>
<p>(
<bold>a</bold>
) The number (mean ± SE, n = 6–10) of macropterous BPH female and male adults in H-tube tests between healthy rice plants and rice plants infected by
<italic>Xoo</italic>
at different days. (
<bold>b</bold>
) The number (mean ± SE, n = 7–9) of
<italic>C. lividipennis</italic>
adults in H-tube tests between healthy rice plants and rice plants infected by
<italic>Xoo</italic>
at different days. (
<bold>c</bold>
) The number (mean ± SE, n = 6–8) of
<italic>C. lividipennis</italic>
adults in H-tube tests between healthy rice plants and rice plants infected by
<italic>Xoo</italic>
after fed by BPH. PI: plants infected by
<italic>Xoo</italic>
. CL:
<italic>C. lividipennis</italic>
. Asterisks show significant differences among the treatments (*
<italic>p</italic>
 < 0.05; **
<italic>p</italic>
 < 0.01).</p>
</caption>
<graphic xlink:href="srep26043-f5"></graphic>
</fig>
<fig id="f6">
<label>Figure 6</label>
<caption>
<title>The amounts of volatile compounds (% of internal standard + SEM, n = 3–4) emitted from health rice and rice infected by
<italic>Xoo</italic>
at 5 d,10 d and 15 d.</title>
<p>PI: plants infected by
<italic>Xoo</italic>
. (
<bold>a</bold>
) Terpenes. (
<bold>b</bold>
) Aldehyde, ketone and esters. Asterisks show significant differences among the treatments (*
<italic>p</italic>
 < 0.05; **
<italic>p</italic>
 < 0.01).</p>
</caption>
<graphic xlink:href="srep26043-f6"></graphic>
</fig>
<fig id="f7">
<label>Figure 7</label>
<caption>
<title>The amounts of volatile compounds (% of IS peak area + SEM, n = 3–5)emitted from healthy rice induced by BPH feed and rice infected by
<italic>Xoo</italic>
at 5 d,10 d and 15 d, meanwhile, have suffer from BPH feed for 24 h.</title>
<p>PI: plants infected by
<italic>Xoo</italic>
. (
<bold>a</bold>
) Terpenes. (
<bold>b</bold>
) Aldehyde, ketone and esters. Asterisks show significant differences among the treatments (*
<italic>p</italic>
 < 0.05; **
<italic>p</italic>
 < 0.01). Some materials didn’t appear in this figure, because they were too few to detect in these sample.</p>
</caption>
<graphic xlink:href="srep26043-f7"></graphic>
</fig>
<fig id="f8">
<label>Figure 8</label>
<caption>
<title>Disease symptoms of bacterial blight.</title>
<p>(
<bold>a</bold>
) The control rice flag leaf. (
<bold>b–d</bold>
) Disease symptoms of bacterial blight at 5, 10, 15 days post inoculation with
<italic>Xanthomonas oryzae</italic>
pv.
<italic>oryzae</italic>
(
<italic>Xoo</italic>
), respectively.</p>
</caption>
<graphic xlink:href="srep26043-f8"></graphic>
</fig>
<table-wrap position="float" id="t1">
<label>Table 1</label>
<caption>
<title>Fecundity and hatchability of BPH on infected rice and control rice plants.</title>
</caption>
<table frame="hsides" rules="groups" border="1">
<colgroup>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom">
<tr>
<th align="left" valign="top" charoff="50"> </th>
<th align="center" valign="top" charoff="50">Rice plants infected by
<italic>Xoo</italic>
</th>
<th align="center" valign="top" charoff="50">Healthy rice plants</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left" valign="top" charoff="50">Number. of the Egg</td>
<td align="center" valign="top" charoff="50">474.94 ± 33.87</td>
<td align="center" valign="top" charoff="50">440.61 ± 39.35</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">Hatching rate (%)</td>
<td align="center" valign="top" charoff="50">63.62 ± 10.75</td>
<td align="center" valign="top" charoff="50">63.89 ± 7.66</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn id="t1-fn1">
<p>Note: The number of BPH eggs (mean ± SE, n = 6, 2 female and 2 male BPH adults oviposited for 10 days). Hatching rate of BPH (mean ± SE, n = 6).</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>

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