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Comparative transcriptome and proteome analysis to reveal the biosynthesis of gold nanoparticles in Arabidopsis

Identifieur interne : 000456 ( Pmc/Curation ); précédent : 000455; suivant : 000457

Comparative transcriptome and proteome analysis to reveal the biosynthesis of gold nanoparticles in Arabidopsis

Auteurs : Manish Tiwari [États-Unis] ; Sneha Krishnamurthy [États-Unis] ; Devesh Shukla [États-Unis] ; Jeffrey Kiiskila [États-Unis] ; Ajay Jain [Inde] ; Rupali Datta [États-Unis] ; Nilesh Sharma [États-Unis] ; Shivendra V. Sahi [États-Unis]

Source :

RBID : PMC:4763195

Abstract

A large number of plants have been tested and exploited in search of a green chemistry approach for the fabrication of gold or other precious metal nanomaterials. Despite the potential of plant based methods, very little is known about the underlying biochemical reactions and genes involved in the biotransformation mechanism of AuCl4 into gold nanoparticles (AuNPs). In this research, we thus focused on studying the effect of Au on growth and nanoparticles formation by analyses of transcriptome, proteome and ionome shift in Arabidopsis. Au exposure favored the growth of Arabidopsis seedling and induced formation of nanoparticles in root and shoot, as indicated by optical and hyperspectral imaging. Root transcriptome analysis demonstrated the differential expression of the members of WRKY, MYB and BHLH gene families, which are involved in the Fe and other essential metals homeostasis. The proteome analysis revealed that Glutathione S-transferases were induced in the shoot and suggested its potential role in the biosynthesis AuNPs. This study also demonstrated the role of plant hormone auxin in determining the Au induced root system architecture. This is the first study using an integrated approach to understand the in planta biotransformation of KAuCl4 into AuNPs.


Url:
DOI: 10.1038/srep21733
PubMed: 26902325
PubMed Central: 4763195

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PMC:4763195

Le document en format XML

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<institution>Department of Biology, Western Kentucky University, 1906 College heights, Bowling Green</institution>
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<p>A large number of plants have been tested and exploited in search of a green chemistry approach for the fabrication of gold or other precious metal nanomaterials. Despite the potential of plant based methods, very little is known about the underlying biochemical reactions and genes involved in the biotransformation mechanism of AuCl
<sub>4</sub>
into gold nanoparticles (AuNPs). In this research, we thus focused on studying the effect of Au on growth and nanoparticles formation by analyses of transcriptome, proteome and ionome shift in
<italic>Arabidopsis</italic>
. Au exposure favored the growth of
<italic>Arabidopsis</italic>
seedling and induced formation of nanoparticles in root and shoot, as indicated by optical and hyperspectral imaging. Root transcriptome analysis demonstrated the differential expression of the members of
<italic>WRKY</italic>
,
<italic>MYB</italic>
and
<italic>BHLH</italic>
gene families, which are involved in the Fe and other essential metals homeostasis. The proteome analysis revealed that Glutathione S-transferases were induced in the shoot and suggested its potential role in the biosynthesis AuNPs. This study also demonstrated the role of plant hormone auxin in determining the Au induced root system architecture. This is the first study using an integrated approach to understand the
<italic>in planta</italic>
biotransformation of KAuCl
<sub>4</sub>
into AuNPs.</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">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">26902325</article-id>
<article-id pub-id-type="pmc">4763195</article-id>
<article-id pub-id-type="pii">srep21733</article-id>
<article-id pub-id-type="doi">10.1038/srep21733</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Comparative transcriptome and proteome analysis to reveal the biosynthesis of gold nanoparticles in Arabidopsis</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Tiwari</surname>
<given-names>Manish</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Krishnamurthy</surname>
<given-names>Sneha</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shukla</surname>
<given-names>Devesh</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kiiskila</surname>
<given-names>Jeffrey</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jain</surname>
<given-names>Ajay</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Datta</surname>
<given-names>Rupali</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sharma</surname>
<given-names>Nilesh</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sahi</surname>
<given-names>Shivendra V.</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>Department of Biology, Western Kentucky University, 1906 College heights, Bowling Green</institution>
, 42101-1080 Kentucky,
<country>USA</country>
</aff>
<aff id="a2">
<label>2</label>
<institution>Department of Biological Sciences, Michigan Technological University</institution>
, Houghton, Michigan,
<country>USA</country>
</aff>
<aff id="a3">
<label>3</label>
<institution>National Research Centre on Plant Biotechnology, Lal Bahadur Shastri Building, Pusa Campus</institution>
, New Delhi, 110012,
<country>India</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="c1">
<label>a</label>
<email>shiv.sahi@wku.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>23</day>
<month>02</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>6</volume>
<elocation-id>21733</elocation-id>
<history>
<date date-type="received">
<day>25</day>
<month>10</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>29</day>
<month>01</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>A large number of plants have been tested and exploited in search of a green chemistry approach for the fabrication of gold or other precious metal nanomaterials. Despite the potential of plant based methods, very little is known about the underlying biochemical reactions and genes involved in the biotransformation mechanism of AuCl
<sub>4</sub>
into gold nanoparticles (AuNPs). In this research, we thus focused on studying the effect of Au on growth and nanoparticles formation by analyses of transcriptome, proteome and ionome shift in
<italic>Arabidopsis</italic>
. Au exposure favored the growth of
<italic>Arabidopsis</italic>
seedling and induced formation of nanoparticles in root and shoot, as indicated by optical and hyperspectral imaging. Root transcriptome analysis demonstrated the differential expression of the members of
<italic>WRKY</italic>
,
<italic>MYB</italic>
and
<italic>BHLH</italic>
gene families, which are involved in the Fe and other essential metals homeostasis. The proteome analysis revealed that Glutathione S-transferases were induced in the shoot and suggested its potential role in the biosynthesis AuNPs. This study also demonstrated the role of plant hormone auxin in determining the Au induced root system architecture. This is the first study using an integrated approach to understand the
<italic>in planta</italic>
biotransformation of KAuCl
<sub>4</sub>
into AuNPs.</p>
</abstract>
</article-meta>
</front>
<floats-group>
<fig id="f1">
<label>Figure 1</label>
<caption>
<title>Effects of Au on morphology of Arabidopsis seedling.</title>
<p>Five days old germinated plants transferred on nutrient rich MS medium (NR) and MS supplemented with 10 ppm Au (NR-Au) and allowed to grow for one week under hydroponic conditions. (
<bold>A</bold>
) Image showing all the rosette leaves of individual seedling grown under NR and NR-Au media. Red square is equivalent to 1 mm
<xref ref-type="bibr" rid="b2">2</xref>
on scale. (
<bold>B</bold>
) Total shoot area of individual seedlings grown under indicated media. (
<bold>C</bold>
) Root system architecture of representative plant shown in (
<bold>A</bold>
). (
<bold>D</bold>
) Measurement of root parameters like primary root length, (
<bold>E</bold>
) lateral root numbers and (F) second order lateral root numbers. Data are presented as ± SEM (n = 12–15). Significance was determined by Student’s unpaired t-test P ≤ 0.05–0.001. *, ** and ***represent significantly difference from NR (P > 0.01, P > 0.001 and P > 0.0001 respectively).</p>
</caption>
<graphic xlink:href="srep21733-f1"></graphic>
</fig>
<fig id="f2">
<label>Figure 2</label>
<caption>
<title>High contrast dark-field imaging for detection of AuNPs in tissues of Arabidopsis.</title>
<p>Images were taken in root of untreated seedling (
<bold>A</bold>
), Au (10 ppm) exposed root (
<bold>B</bold>
), control shoot (
<bold>C</bold>
) and Au (10 ppm) exposed shoot (
<bold>D</bold>
). Red spots display the distribution of AuNPs in cells and marked with red circle for better visualization.</p>
</caption>
<graphic xlink:href="srep21733-f2"></graphic>
</fig>
<fig id="f3">
<label>Figure 3</label>
<caption>
<title>Plant Gene Set Enrichment Analysis of significantly upregulated genes.</title>
</caption>
<graphic xlink:href="srep21733-f3"></graphic>
</fig>
<fig id="f4">
<label>Figure 4</label>
<caption>
<title>Expression of genes in the shoot of
<italic>Arabidopsis</italic>
after Au treatment.</title>
</caption>
<graphic xlink:href="srep21733-f4"></graphic>
</fig>
<fig id="f5">
<label>Figure 5</label>
<caption>
<title>The 2D gel analysis of proteins extracted from root and shoot.</title>
<p>The numbers assigned to the proteins spots correspond to listed in
<xref ref-type="table" rid="t2">Table 2</xref>
. The 2D gel electrophoresis picture showing the root (
<bold>A</bold>
) and shoot (
<bold>B</bold>
). The protein spots with significant differential expressions used in MALDI-TOF MS analysis were encircled.</p>
</caption>
<graphic xlink:href="srep21733-f5"></graphic>
</fig>
<fig id="f6">
<label>Figure 6</label>
<caption>
<title>Quantification of essential metals in root and shoot of
<italic>Arabidopsis</italic>
.</title>
<p>NR denotes for nutrient rich MS media whereas NR-Au for media supplemented with 10 ppm Au. Significance was determined by Student’s unpaired t-test P ≤ 0.05–0.001. ***and ***represent significantly difference from NR (P > 0.01, P > 0.001 and P > 0.0001 respectively).</p>
</caption>
<graphic xlink:href="srep21733-f6"></graphic>
</fig>
<table-wrap position="float" id="t1">
<label>Table 1</label>
<caption>
<title>Comparison of microarray data by quantitative RT-PCR.</title>
</caption>
<table frame="hsides" rules="groups" border="1">
<colgroup>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom">
<tr>
<th rowspan="2" align="left" valign="top" charoff="50">Locus ID</th>
<th rowspan="2" align="center" valign="top" charoff="50">Annotation</th>
<th align="center" valign="top" charoff="50">Microarray</th>
<th align="center" valign="top" charoff="50">qRT-PCR</th>
<th rowspan="2" align="center" valign="top" charoff="50">25 ppm Au (Fold change)</th>
</tr>
<tr>
<th align="center" valign="top" charoff="50">(Fold change)</th>
<th align="center" valign="top" charoff="50">10 ppm Au (Fold change)</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left" valign="top" charoff="50">AT5G23990</td>
<td align="center" valign="top" charoff="50">FRO5</td>
<td align="center" valign="top" charoff="50">17.54</td>
<td align="center" valign="top" charoff="50">7.269</td>
<td align="center" valign="top" charoff="50">1.855</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT2G46830</td>
<td align="center" valign="top" charoff="50">CCA1</td>
<td align="center" valign="top" charoff="50">3.88</td>
<td align="center" valign="top" charoff="50">4.645</td>
<td align="center" valign="top" charoff="50">0.472</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT1G63950</td>
<td align="center" valign="top" charoff="50">HMA3</td>
<td align="center" valign="top" charoff="50">3.833</td>
<td align="center" valign="top" charoff="50">26.459</td>
<td align="center" valign="top" charoff="50">0.025</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT3G28345</td>
<td align="center" valign="top" charoff="50">ABC transporter B family member</td>
<td align="center" valign="top" charoff="50">3.102</td>
<td align="center" valign="top" charoff="50">2.215</td>
<td align="center" valign="top" charoff="50">0.526</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT5G14570</td>
<td align="center" valign="top" charoff="50">High affinity nitrate transporter</td>
<td align="center" valign="top" charoff="50">3.4</td>
<td align="center" valign="top" charoff="50">2.250</td>
<td align="center" valign="top" charoff="50">2.406</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT3G46900</td>
<td align="center" valign="top" charoff="50">COPT2</td>
<td align="center" valign="top" charoff="50">4.22</td>
<td align="center" valign="top" charoff="50">4.835</td>
<td align="center" valign="top" charoff="50">1.192</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT1G01060</td>
<td align="center" valign="top" charoff="50">LHY</td>
<td align="center" valign="top" charoff="50">3.59</td>
<td align="center" valign="top" charoff="50">2.978</td>
<td align="center" valign="top" charoff="50">1.638</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT3G12320</td>
<td align="center" valign="top" charoff="50">Light-inducible and clock-regulated 3, LNK3</td>
<td align="center" valign="top" charoff="50">4.81</td>
<td align="center" valign="top" charoff="50">8.889</td>
<td align="center" valign="top" charoff="50">0.498</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT1G33730</td>
<td align="center" valign="top" charoff="50">CYP76C5</td>
<td align="center" valign="top" charoff="50">3.77</td>
<td align="center" valign="top" charoff="50">1.685</td>
<td align="center" valign="top" charoff="50">2.308</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT5G17300</td>
<td align="center" valign="top" charoff="50">RVE1</td>
<td align="center" valign="top" charoff="50">2.919</td>
<td align="center" valign="top" charoff="50">2.689</td>
<td align="center" valign="top" charoff="50">1.986</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT5G24380</td>
<td align="center" valign="top" charoff="50">YSL2</td>
<td align="center" valign="top" charoff="50">3</td>
<td align="center" valign="top" charoff="50">1.332</td>
<td align="center" valign="top" charoff="50">0.386</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT3G09600</td>
<td align="center" valign="top" charoff="50">Myb</td>
<td align="center" valign="top" charoff="50">2.37</td>
<td align="center" valign="top" charoff="50">2.087</td>
<td align="center" valign="top" charoff="50">2.288</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT4G10530</td>
<td align="center" valign="top" charoff="50">Subtilase family protein</td>
<td align="center" valign="top" charoff="50">−6.85</td>
<td align="center" valign="top" charoff="50">0.073</td>
<td align="center" valign="top" charoff="50">0.450</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT5G49770</td>
<td align="center" valign="top" charoff="50">Leucine-rich repeat receptor-like protein kinase</td>
<td align="center" valign="top" charoff="50">−2.79</td>
<td align="center" valign="top" charoff="50">0.183</td>
<td align="center" valign="top" charoff="50">0.385</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">AT2G44840</td>
<td align="center" valign="top" charoff="50">ERF13</td>
<td align="center" valign="top" charoff="50">−2.01</td>
<td align="center" valign="top" charoff="50">0.179</td>
<td align="center" valign="top" charoff="50">1.116</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap position="float" id="t2">
<label>Table 2</label>
<caption>
<title>Au responsive proteins in root and shoot of
<italic>Arabidopsis</italic>
.</title>
</caption>
<table frame="hsides" rules="groups" border="1">
<colgroup>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom">
<tr>
<th align="left" valign="top" charoff="50">Spot ID</th>
<th align="center" valign="top" charoff="50">Tissue</th>
<th align="center" valign="top" charoff="50">Fold change</th>
<th align="center" valign="top" charoff="50">Protein</th>
<th align="center" valign="top" charoff="50">Score</th>
<th align="center" valign="top" charoff="50">Nominal mass (Da)</th>
<th align="center" valign="top" charoff="50">Calculated pI</th>
<th align="center" valign="top" charoff="50">Sequence coverage</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left" valign="top" charoff="50">85</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">7.98</td>
<td align="center" valign="top" charoff="50">Putative inactive cadmium/zinc-transporting ATPase HMA3</td>
<td align="center" valign="top" charoff="50">34</td>
<td align="center" valign="top" charoff="50">59440</td>
<td align="center" valign="top" charoff="50">7.44</td>
<td align="center" valign="top" charoff="50">10%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">33</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">4.76</td>
<td align="center" valign="top" charoff="50">Thioredoxin-like protein HCF164, chloroplastic</td>
<td align="center" valign="top" charoff="50">23</td>
<td align="center" valign="top" charoff="50">28916</td>
<td align="center" valign="top" charoff="50">5.26</td>
<td align="center" valign="top" charoff="50">6%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">4X</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">3.50</td>
<td align="center" valign="top" charoff="50">UDP-glycosyltransferase 90A1</td>
<td align="center" valign="top" charoff="50">27</td>
<td align="center" valign="top" charoff="50">54055</td>
<td align="center" valign="top" charoff="50">5.65</td>
<td align="center" valign="top" charoff="50">5%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">56</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">2.99</td>
<td align="center" valign="top" charoff="50">Probable fructokinase-1</td>
<td align="center" valign="top" charoff="50">52</td>
<td align="center" valign="top" charoff="50">35424</td>
<td align="center" valign="top" charoff="50">5.31</td>
<td align="center" valign="top" charoff="50">20%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">67</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">2.56</td>
<td align="center" valign="top" charoff="50">Glyceraldehyde-3-phosphate dehydrogenase GAPC1, cytosolic</td>
<td align="center" valign="top" charoff="50">55</td>
<td align="center" valign="top" charoff="50">37028</td>
<td align="center" valign="top" charoff="50">6.62</td>
<td align="center" valign="top" charoff="50">27%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">7X</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">2.55</td>
<td align="center" valign="top" charoff="50">UDP-glycosyltransferase 73C5</td>
<td align="center" valign="top" charoff="50">31</td>
<td align="center" valign="top" charoff="50">56390</td>
<td align="center" valign="top" charoff="50">5.38</td>
<td align="center" valign="top" charoff="50">8%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">36</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">2.54</td>
<td align="center" valign="top" charoff="50">High mobility group B protein 7</td>
<td align="center" valign="top" charoff="50">33</td>
<td align="center" valign="top" charoff="50">27136</td>
<td align="center" valign="top" charoff="50">4.83</td>
<td align="center" valign="top" charoff="50">10%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">21</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">−2.19</td>
<td align="center" valign="top" charoff="50">Superoxide dismutase [Mn] 1, mitochondrial</td>
<td align="center" valign="top" charoff="50">32</td>
<td align="center" valign="top" charoff="50">25485</td>
<td align="center" valign="top" charoff="50">8.47</td>
<td align="center" valign="top" charoff="50">41%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">28</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">−2.73</td>
<td align="center" valign="top" charoff="50">Glutathione S-transferase F6</td>
<td align="center" valign="top" charoff="50">12</td>
<td align="center" valign="top" charoff="50">23471</td>
<td align="center" valign="top" charoff="50">5.8</td>
<td align="center" valign="top" charoff="50">15%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">12</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">−3.62</td>
<td align="center" valign="top" charoff="50">40S ribosomal protein S15-6</td>
<td align="center" valign="top" charoff="50">33</td>
<td align="center" valign="top" charoff="50">18849</td>
<td align="center" valign="top" charoff="50">10.59</td>
<td align="center" valign="top" charoff="50">21%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">71</td>
<td align="center" valign="top" charoff="50">Root</td>
<td align="center" valign="top" charoff="50">−5.67</td>
<td align="center" valign="top" charoff="50">Vesicle-associated protein 2−2</td>
<td align="center" valign="top" charoff="50">26</td>
<td align="center" valign="top" charoff="50">43527</td>
<td align="center" valign="top" charoff="50">6.54</td>
<td align="center" valign="top" charoff="50">27%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">67</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">6.07</td>
<td align="center" valign="top" charoff="50">Thioredoxin domain-containing protein PLP3B</td>
<td align="center" valign="top" charoff="50">28</td>
<td align="center" valign="top" charoff="50">26522</td>
<td align="center" valign="top" charoff="50">5.54</td>
<td align="center" valign="top" charoff="50">9%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">43</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">5.50</td>
<td align="center" valign="top" charoff="50">Pentatricopeptide repeat-containing protein At1g62350</td>
<td align="center" valign="top" charoff="50">27</td>
<td align="center" valign="top" charoff="50">23386</td>
<td align="center" valign="top" charoff="50">5.05</td>
<td align="center" valign="top" charoff="50">23%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">101</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">4.02</td>
<td align="center" valign="top" charoff="50">Glycerophosphodiester phosphodiesterase GDPD3</td>
<td align="center" valign="top" charoff="50">31</td>
<td align="center" valign="top" charoff="50">42665</td>
<td align="center" valign="top" charoff="50">5.12</td>
<td align="center" valign="top" charoff="50">21%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">63</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">3.47</td>
<td align="center" valign="top" charoff="50">Glutathione S-transferase U21</td>
<td align="center" valign="top" charoff="50">20</td>
<td align="center" valign="top" charoff="50">25857</td>
<td align="center" valign="top" charoff="50">5.42</td>
<td align="center" valign="top" charoff="50">18%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">85</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">3.24</td>
<td align="center" valign="top" charoff="50">Probable 3-hydroxyisobutyrate dehydrogenase-like 3, mitochondrial</td>
<td align="center" valign="top" charoff="50">42</td>
<td align="center" valign="top" charoff="50">33549</td>
<td align="center" valign="top" charoff="50">6.34</td>
<td align="center" valign="top" charoff="50">27%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">65</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">3.00</td>
<td align="center" valign="top" charoff="50">Glutathione S-transferase U15</td>
<td align="center" valign="top" charoff="50">30</td>
<td align="center" valign="top" charoff="50">26689</td>
<td align="center" valign="top" charoff="50">5.46</td>
<td align="center" valign="top" charoff="50">21%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">13</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.90</td>
<td align="center" valign="top" charoff="50">U11/U12 small nuclear ribonucleoprotein 25 kDa protein</td>
<td align="center" valign="top" charoff="50">34</td>
<td align="center" valign="top" charoff="50">18775</td>
<td align="center" valign="top" charoff="50">9.75</td>
<td align="center" valign="top" charoff="50">32%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">42</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.89</td>
<td align="center" valign="top" charoff="50">Lactoylglutathione lyase</td>
<td align="center" valign="top" charoff="50">20</td>
<td align="center" valign="top" charoff="50">20892</td>
<td align="center" valign="top" charoff="50">5.14</td>
<td align="center" valign="top" charoff="50">15%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">46</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.72</td>
<td align="center" valign="top" charoff="50">Glutathione S-transferase F2</td>
<td align="center" valign="top" charoff="50">65</td>
<td align="center" valign="top" charoff="50">24114</td>
<td align="center" valign="top" charoff="50">5.92</td>
<td align="center" valign="top" charoff="50">37%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">37</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.60</td>
<td align="center" valign="top" charoff="50">PRA1 family protein G2</td>
<td align="center" valign="top" charoff="50">43</td>
<td align="center" valign="top" charoff="50">20633</td>
<td align="center" valign="top" charoff="50">5.15</td>
<td align="center" valign="top" charoff="50">24%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">4</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.55</td>
<td align="center" valign="top" charoff="50">NADH dehydrogenase [ubiquinone] 1 beta subcomplex subunit 9</td>
<td align="center" valign="top" charoff="50">38</td>
<td align="center" valign="top" charoff="50">13665</td>
<td align="center" valign="top" charoff="50">8.74</td>
<td align="center" valign="top" charoff="50">58%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">7</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.44</td>
<td align="center" valign="top" charoff="50">Cytochrome c oxidase subunit 5b-1, mitochondrial</td>
<td align="center" valign="top" charoff="50">47</td>
<td align="center" valign="top" charoff="50">19575</td>
<td align="center" valign="top" charoff="50">4.91</td>
<td align="center" valign="top" charoff="50">20%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">98</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.43</td>
<td align="center" valign="top" charoff="50">F-box protein PP2-A15</td>
<td align="center" valign="top" charoff="50">22</td>
<td align="center" valign="top" charoff="50">34631</td>
<td align="center" valign="top" charoff="50">6.16</td>
<td align="center" valign="top" charoff="50">21%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">34</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">2.00</td>
<td align="center" valign="top" charoff="50">Auxin-responsive protein IAA5</td>
<td align="center" valign="top" charoff="50">20</td>
<td align="center" valign="top" charoff="50">18741</td>
<td align="center" valign="top" charoff="50">6.37</td>
<td align="center" valign="top" charoff="50">41%</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">107</td>
<td align="center" valign="top" charoff="50">Shoot</td>
<td align="center" valign="top" charoff="50">−3.44</td>
<td align="center" valign="top" charoff="50">Serine racemase</td>
<td align="center" valign="top" charoff="50">27</td>
<td align="center" valign="top" charoff="50">35524</td>
<td align="center" valign="top" charoff="50">6.95</td>
<td align="center" valign="top" charoff="50">23%</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
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