Metabolomic-Based Study of the Leafy Gall, the Ecological Niche of the Phytopathogen Rhodococcus Fascians, as a Potential Source of Bioactive Compounds
Identifieur interne : 000134 ( Pmc/Checkpoint ); précédent : 000133; suivant : 000135Metabolomic-Based Study of the Leafy Gall, the Ecological Niche of the Phytopathogen Rhodococcus Fascians, as a Potential Source of Bioactive Compounds
Auteurs : Aminata P. Nacoulma ; Olivier M. Vandeputte ; Manuella De Lorenzi ; Mondher El Jaziri ; Pierre DuezSource :
- International Journal of Molecular Sciences [ 1422-0067 ] ; 2013.
Abstract
Leafy gall is a plant hyperplasia induced upon
Url:
DOI: 10.3390/ijms140612533
PubMed: 23771021
PubMed Central: 3709798
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Metabolomic-Based Study of the Leafy Gall, the Ecological Niche of the Phytopathogen <italic>Rhodococcus Fascians</italic>, as a Potential Source of Bioactive Compounds</title><author><name sortKey="Nacoulma, Aminata P" sort="Nacoulma, Aminata P" uniqKey="Nacoulma A" first="Aminata P." last="Nacoulma">Aminata P. Nacoulma</name><affiliation><nlm:aff id="af1-ijms-14-12533">Laboratory of Toxicology, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/1, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>manuela.de.lorenzi@ulb.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="Vandeputte, Olivier M" sort="Vandeputte, Olivier M" uniqKey="Vandeputte O" first="Olivier M." last="Vandeputte">Olivier M. Vandeputte</name><affiliation><nlm:aff id="af2-ijms-14-12533">Laboratory of Plant Biotechnology, Faculty of Sciences, Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, Gosselies B-6041, Belgium; E-Mails:<email>olivier.vandeputte@ulb.ac.be</email> (O.M.V.);<email>jaziri@ulb.ac.be</email> (M.E.J.)</nlm:aff></affiliation></author><author><name sortKey="De Lorenzi, Manuella" sort="De Lorenzi, Manuella" uniqKey="De Lorenzi M" first="Manuella" last="De Lorenzi">Manuella De Lorenzi</name><affiliation><nlm:aff id="af1-ijms-14-12533">Laboratory of Toxicology, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/1, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>manuela.de.lorenzi@ulb.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="El Jaziri, Mondher" sort="El Jaziri, Mondher" uniqKey="El Jaziri M" first="Mondher" last="El Jaziri">Mondher El Jaziri</name><affiliation><nlm:aff id="af2-ijms-14-12533">Laboratory of Plant Biotechnology, Faculty of Sciences, Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, Gosselies B-6041, Belgium; E-Mails:<email>olivier.vandeputte@ulb.ac.be</email> (O.M.V.);<email>jaziri@ulb.ac.be</email> (M.E.J.)</nlm:aff></affiliation></author><author><name sortKey="Duez, Pierre" sort="Duez, Pierre" uniqKey="Duez P" first="Pierre" last="Duez">Pierre Duez</name><affiliation><nlm:aff id="af3-ijms-14-12533">Laboratory of Pharmacognosy, Bromatology and Human Nutrition, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/9, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>pduez@ulb.ac.be</email></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23771021</idno><idno type="pmc">3709798</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3709798</idno><idno type="RBID">PMC:3709798</idno><idno type="doi">10.3390/ijms140612533</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">000185</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000185</idno><idno type="wicri:Area/Pmc/Curation">000185</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000185</idno><idno type="wicri:Area/Pmc/Checkpoint">000134</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000134</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Metabolomic-Based Study of the Leafy Gall, the Ecological Niche of the Phytopathogen <italic>Rhodococcus Fascians</italic>, as a Potential Source of Bioactive Compounds</title><author><name sortKey="Nacoulma, Aminata P" sort="Nacoulma, Aminata P" uniqKey="Nacoulma A" first="Aminata P." last="Nacoulma">Aminata P. Nacoulma</name><affiliation><nlm:aff id="af1-ijms-14-12533">Laboratory of Toxicology, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/1, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>manuela.de.lorenzi@ulb.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="Vandeputte, Olivier M" sort="Vandeputte, Olivier M" uniqKey="Vandeputte O" first="Olivier M." last="Vandeputte">Olivier M. Vandeputte</name><affiliation><nlm:aff id="af2-ijms-14-12533">Laboratory of Plant Biotechnology, Faculty of Sciences, Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, Gosselies B-6041, Belgium; E-Mails:<email>olivier.vandeputte@ulb.ac.be</email> (O.M.V.);<email>jaziri@ulb.ac.be</email> (M.E.J.)</nlm:aff></affiliation></author><author><name sortKey="De Lorenzi, Manuella" sort="De Lorenzi, Manuella" uniqKey="De Lorenzi M" first="Manuella" last="De Lorenzi">Manuella De Lorenzi</name><affiliation><nlm:aff id="af1-ijms-14-12533">Laboratory of Toxicology, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/1, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>manuela.de.lorenzi@ulb.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="El Jaziri, Mondher" sort="El Jaziri, Mondher" uniqKey="El Jaziri M" first="Mondher" last="El Jaziri">Mondher El Jaziri</name><affiliation><nlm:aff id="af2-ijms-14-12533">Laboratory of Plant Biotechnology, Faculty of Sciences, Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, Gosselies B-6041, Belgium; E-Mails:<email>olivier.vandeputte@ulb.ac.be</email> (O.M.V.);<email>jaziri@ulb.ac.be</email> (M.E.J.)</nlm:aff></affiliation></author><author><name sortKey="Duez, Pierre" sort="Duez, Pierre" uniqKey="Duez P" first="Pierre" last="Duez">Pierre Duez</name><affiliation><nlm:aff id="af3-ijms-14-12533">Laboratory of Pharmacognosy, Bromatology and Human Nutrition, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/9, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>pduez@ulb.ac.be</email></nlm:aff></affiliation></author></analytic><series><title level="j">International Journal of Molecular Sciences</title><idno type="eISSN">1422-0067</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Leafy gall is a plant hyperplasia induced upon <italic>Rhodococcus fascians</italic> infection. Previously, by genomic and transcriptomic analysis, it has been reported that, at the early stage of symptom development, both primary and secondary metabolisms are modified. The present study is based on the hypothesis that fully developed leafy gall, could represent a potential source of new bioactive compounds. Therefore, non-targeted metabolomic analysis of aqueous and chloroform extracts of leafy gall and non-infected tobacco was carried out by <sup>1</sup>H-NMR coupled to principal component analysis (PCA) and orthogonal projections to latent structures-discriminant analysis (OPLS-DA). Polar metabolite profiling reflects modifications mainly in the primary metabolites and in some polyphenolics. In contrast, main modifications occurring in non-polar metabolites concern secondary metabolites, and gas chromatography and mass spectrometry (GC-MS) evidenced alterations in diterpenoids family. Analysis of crude extracts of leafy galls and non-infected tobacco leaves exhibited a distinct antiproliferative activity against all four tested human cancer cell lines. A bio-guided fractionation of chloroformic crude extract yield to semi-purified fractions, which inhibited proliferation of glioblastoma U373 cells with IC<sub>50</sub> between 14.0 and 2.4 μg/mL. Discussion is focused on the consequence of these metabolic changes, with respect to plant defense mechanisms following infection. Considering the promising role of diterpenoid family as bioactive compounds, leafy gall may rather be a propitious source for drug discovery.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Agrios, G N" uniqKey="Agrios G">G.N. Agrios</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hayward, A" uniqKey="Hayward A">A. Hayward</name></author><author><name sortKey="Stone, G" uniqKey="Stone G">G. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Mol Sci</journal-id><journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id><journal-id journal-id-type="publisher-id">ijms</journal-id><journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title></journal-title-group><issn pub-type="epub">1422-0067</issn><publisher><publisher-name>Molecular Diversity Preservation International (MDPI)</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23771021</article-id><article-id pub-id-type="pmc">3709798</article-id><article-id pub-id-type="doi">10.3390/ijms140612533</article-id><article-id pub-id-type="publisher-id">ijms-14-12533</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Metabolomic-Based Study of the Leafy Gall, the Ecological Niche of the Phytopathogen <italic>Rhodococcus Fascians</italic>, as a Potential Source of Bioactive Compounds</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Nacoulma</surname><given-names>Aminata P.</given-names></name><xref ref-type="aff" rid="af1-ijms-14-12533">1</xref><xref rid="c1-ijms-14-12533" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Vandeputte</surname><given-names>Olivier M.</given-names></name><xref ref-type="aff" rid="af2-ijms-14-12533">2</xref></contrib><contrib contrib-type="author"><name><surname>De Lorenzi</surname><given-names>Manuella</given-names></name><xref ref-type="aff" rid="af1-ijms-14-12533">1</xref></contrib><contrib contrib-type="author"><name><surname>El Jaziri</surname><given-names>Mondher</given-names></name><xref ref-type="aff" rid="af2-ijms-14-12533">2</xref></contrib><contrib contrib-type="author"><name><surname>Duez</surname><given-names>Pierre</given-names></name><xref ref-type="aff" rid="af3-ijms-14-12533">3</xref></contrib></contrib-group><aff id="af1-ijms-14-12533"><label>1</label>Laboratory of Toxicology, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/1, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>manuela.de.lorenzi@ulb.ac.be</email></aff><aff id="af2-ijms-14-12533"><label>2</label>Laboratory of Plant Biotechnology, Faculty of Sciences, Université Libre de Bruxelles, 12 rue des Professeurs Jeener et Brachet, Gosselies B-6041, Belgium; E-Mails:<email>olivier.vandeputte@ulb.ac.be</email> (O.M.V.);<email>jaziri@ulb.ac.be</email> (M.E.J.)</aff><aff id="af3-ijms-14-12533"><label>3</label>Laboratory of Pharmacognosy, Bromatology and Human Nutrition, Faculty of Pharmacy, Université Libre de Bruxelles, CP 205/9, Boulevard du Triomphe, Brussels B-1050, Belgium; E-Mail:<email>pduez@ulb.ac.be</email></aff><author-notes><corresp id="c1-ijms-14-12533"><label>*</label>Author to whom correspondence should be addressed; E-Mail: <email>aminata.nacoulma@ulb.ac.be</email>; Tel./Fax: +32-2650-5174.</corresp></author-notes><pub-date pub-type="collection"><month>6</month><year>2013</year></pub-date><pub-date pub-type="epub"><day>14</day><month>6</month><year>2013</year></pub-date><volume>14</volume><issue>6</issue><fpage>12533</fpage><lpage>12549</lpage><history><date date-type="received"><day>22</day><month>4</month><year>2013</year></date><date date-type="rev-recd"><day>21</day><month>5</month><year>2013</year></date><date date-type="accepted"><day>04</day><month>6</month><year>2013</year></date></history><permissions><copyright-statement>© 2013 by the authors; licensee MDPI, Basel, Switzerland</copyright-statement><copyright-year>2013</copyright-year><license license-type="open-access"><license-p>This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>).</license-p></license></permissions><abstract><p>Leafy gall is a plant hyperplasia induced upon <italic>Rhodococcus fascians</italic> infection. Previously, by genomic and transcriptomic analysis, it has been reported that, at the early stage of symptom development, both primary and secondary metabolisms are modified. The present study is based on the hypothesis that fully developed leafy gall, could represent a potential source of new bioactive compounds. Therefore, non-targeted metabolomic analysis of aqueous and chloroform extracts of leafy gall and non-infected tobacco was carried out by <sup>1</sup>H-NMR coupled to principal component analysis (PCA) and orthogonal projections to latent structures-discriminant analysis (OPLS-DA). Polar metabolite profiling reflects modifications mainly in the primary metabolites and in some polyphenolics. In contrast, main modifications occurring in non-polar metabolites concern secondary metabolites, and gas chromatography and mass spectrometry (GC-MS) evidenced alterations in diterpenoids family. Analysis of crude extracts of leafy galls and non-infected tobacco leaves exhibited a distinct antiproliferative activity against all four tested human cancer cell lines. A bio-guided fractionation of chloroformic crude extract yield to semi-purified fractions, which inhibited proliferation of glioblastoma U373 cells with IC<sub>50</sub> between 14.0 and 2.4 μg/mL. Discussion is focused on the consequence of these metabolic changes, with respect to plant defense mechanisms following infection. Considering the promising role of diterpenoid family as bioactive compounds, leafy gall may rather be a propitious source for drug discovery.</p></abstract><kwd-group><kwd>metabolomics</kwd><kwd>tobacco</kwd><kwd>multivariate data analysis</kwd><kwd>diterpenoids</kwd><kwd>leafy gall</kwd><kwd><italic>Rhodococcus fascians</italic></kwd></kwd-group></article-meta></front><floats-group><fig id="f1-ijms-14-12533" position="float"><label>Figure 1</label><caption><p>The morphological features of leafy gall (LG) formed in <italic>Rhodococcus fascians</italic>-infected tobacco plant (eight weeks post infection) and non-infected (NI) tobacco plant grown for 12 weeks. The <italic>in vitro</italic> tobacco plants were infected four weeks post germination. Bar = 1 cm.</p></caption><graphic xlink:href="ijms-14-12533f1"></graphic></fig><fig id="f2-ijms-14-12533" position="float"><label>Figure 2</label><caption><p>The typical <sup>1</sup>H-NMR spectra (300.13 MHz) of non-polar tobacco metabolites from NI and LG tissues. Zoom-ups of the aliphatic (0.5–3.0 ppm) and olefinic (5.0–5.5 ppm) regions are included.</p></caption><graphic xlink:href="ijms-14-12533f2"></graphic></fig><fig id="f3-ijms-14-12533" position="float"><label>Figure 3</label><caption><p>The typical <sup>1</sup>H-NMR spectra (300.13 MHz) of polar tobacco metabolites from NI and LG infected tissues.</p></caption><graphic xlink:href="ijms-14-12533f3"></graphic></fig><fig id="f4-ijms-14-12533" position="float"><label>Figure 4</label><caption><p>Principal components analysis (PCA) of <sup>1</sup>H-NMR spectra for chloroformic extracts of both LG and NI tobacco tissues; (<bold>a</bold>) The first two components explain 99.7% of the variation (PC1: 78.6% and PC2: 21.1%) with a clear discrimination between LG and NI extracts along PC1; (<bold>b</bold>) Loading plot of the PC1 component shown in <bold>a</bold>. The discrimination between infected and non-infected tobacco plant extracts mainly takes place in the aliphatic region, at δ 0.7–3.0 ppm, and in the olefinic region, at δ 5.0–5.5 ppm. These spectral regions correspond to the signals characteristic of terpenoids and steroids [<xref rid="b21-ijms-14-12533" ref-type="bibr">21</xref>].</p></caption><graphic xlink:href="ijms-14-12533f4"></graphic></fig><fig id="f5-ijms-14-12533" position="float"><label>Figure 5</label><caption><p>The typical GC-MS chromatograms of non-polar tobacco metabolites from NI and LG tobacco tissues. The arrow indicates the gas chromatography and mass spectrometry (GC-MS) peak corresponding to commercially available cembrene. See Material and Methods for chromatographic conditions.</p></caption><graphic xlink:href="ijms-14-12533f5"></graphic></fig><fig id="f6-ijms-14-12533" position="float"><label>Figure 6</label><caption><p>The principal components analysis of <sup>1</sup>H-NMR spectra for aqueous extracts of both NI and LG tobacco tissues; (<bold>a</bold>) The first two components explain 81.5% of the variation (PC1: 62.2% and PC2: 19.3%) with a small discrimination between NI and LG extracts along PC1; (<bold>b</bold>) Loading plot of the PC1 component shown in (a). The discrimination between infected and non-infected tobacco plant extracts mainly takes place at δ 2–5.5 ppm.</p></caption><graphic xlink:href="ijms-14-12533f6"></graphic></fig><fig id="f7-ijms-14-12533" position="float"><label>Figure 7</label><caption><p>The orthogonal projections to latent structures discriminating analysis (OPLS-DA) of <sup>1</sup>H-NMR spectra for aqueous extracts of both NI and <italic>Rhodococcus fascians</italic>-infected LG tobacco tissues; (<bold>a</bold>) The predictive component (Cp, <italic>X</italic>-axis) explains 46.1% and the first orthogonal component (Co1, <italic>Y</italic>-axis) 19.4% of the dataset variation; (<bold>b</bold>) The <italic>X</italic> axis (p) describes the loadings of each variable and <italic>Y</italic>-axis (p(corr)) represents the reliability of each variable in the dataset. Cut-off values for the covariance and the correlation were assigned to <italic>p</italic> > 0.05 and <italic>p</italic>(corr) > 0.5, respectively (S-plot). Metabolites in the upper-right and lower-left quadrants are potential biomarkers, and best discriminate the LG and NI samples with smaller risk for illegitimate correlations (<italic>p</italic> > 0.05); the induced compounds corresponding to discriminant loadings are inferred according to the literature [<xref rid="b21-ijms-14-12533" ref-type="bibr">21</xref>,<xref rid="b30-ijms-14-12533" ref-type="bibr">30</xref>]. These include sugars (raffinose, galactitol), aminoacids (proline, glutamine), organic acids (malic acid), and phenolics (caffeoylquinic acid); (<bold>c</bold>) OPLS-DA variable importance in the projection-plot with confidence intervals of buckets contributing to discriminating LG and NI tobacco plants polar extracts; the arrows indicate the <sup>1</sup>H chemical shifts (ppm) of significant polar metabolites (<xref rid="t3-ijms-14-12533" ref-type="table">Table 3</xref>).</p></caption><graphic xlink:href="ijms-14-12533f7"></graphic></fig><fig id="f8-ijms-14-12533" position="float"><label>Figure 8</label><caption><p>The crude chloroformic extract of tobacco leafy galls contain compounds with antiproliferative activity against the glioblastoma U373 cell line. Schematic overview of the bio-guided fractionation of LG crude extract using the MTT colorimetric cell growth inhibition bioassay. The efficiency of each considered fraction is expressed as the IC<sub>50</sub> value; fractions in bold were analyzed further. The data are presented as the mean ± SD (<italic>n</italic> = 3).</p></caption><graphic xlink:href="ijms-14-12533f8"></graphic></fig><table-wrap id="t1-ijms-14-12533" position="float"><label>Table 1</label><caption><p>The one-way ANOVA analysis of <italic>Rhodococcus. fascians</italic> infected and non-infected tobacco extracts PCA scores based on <sup>1</sup>H-NMR signals changes.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="bottom" rowspan="1" colspan="1">Extracts</th><th align="center" valign="bottom" rowspan="1" colspan="1">DF</th><th align="center" valign="bottom" rowspan="1" colspan="1">F</th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>p</italic>-value</th></tr></thead><tbody><tr><td align="center" valign="top" rowspan="1" colspan="1">Polar metabolites</td><td align="center" valign="top" rowspan="1" colspan="1">8</td><td align="center" valign="top" rowspan="1" colspan="1">0.15</td><td align="center" valign="top" rowspan="1" colspan="1">0.71</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">Non-polar metabolites</td><td align="center" valign="top" rowspan="1" colspan="1">12</td><td align="center" valign="top" rowspan="1" colspan="1">636.3</td><td align="center" valign="top" rowspan="1" colspan="1">4.37 × 10<sup>−11</sup></td></tr></tbody></table><table-wrap-foot><fn id="tfn1-ijms-14-12533"><p>DF: describes the degrees of freedom and F the fisher coefficient.</p></fn></table-wrap-foot></table-wrap><table-wrap id="t2-ijms-14-12533" position="float"><label>Table 2</label><caption><p>The summary of PCA and OPLS-DA models.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="bottom" rowspan="1" colspan="1">Multivariate data analysis models</th><th align="left" valign="bottom" rowspan="1" colspan="1">A</th><th align="left" valign="bottom" rowspan="1" colspan="1"><italic>n</italic></th><th align="left" valign="bottom" rowspan="1" colspan="1"><italic>R</italic><sup>2</sup></th><th align="left" valign="bottom" rowspan="1" colspan="1"><italic>Q</italic><sup>2</sup></th></tr></thead><tbody><tr><td colspan="5" align="left" valign="top" rowspan="1"><bold>PCA</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> <bold>Non-polar metabolites</bold></td><td align="left" valign="top" rowspan="1" colspan="1">3</td><td align="left" valign="top" rowspan="1" colspan="1">13</td><td align="left" valign="top" rowspan="1" colspan="1">0.99</td><td align="left" valign="top" rowspan="1" colspan="1">0.99</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> <bold>Polar metabolites</bold></td><td align="left" valign="top" rowspan="1" colspan="1">6</td><td align="left" valign="top" rowspan="1" colspan="1">9</td><td align="left" valign="top" rowspan="1" colspan="1">0.99</td><td align="left" valign="top" rowspan="1" colspan="1">0.65</td></tr><tr><td colspan="5" align="left" valign="top" rowspan="1"><bold>OPLS-DA</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"> <bold>Polar metabolites</bold></td><td align="left" valign="top" rowspan="1" colspan="1">1+4</td><td align="left" valign="top" rowspan="1" colspan="1">9</td><td align="left" valign="top" rowspan="1" colspan="1">0.98</td><td align="left" valign="top" rowspan="1" colspan="1">0.93</td></tr></tbody></table><table-wrap-foot><fn id="tfn2-ijms-14-12533"><p>A describes the model components; <italic>n</italic>, the number of observations; <italic>R</italic><sup>2</sup>, the total variation explained; <italic>Q</italic><sup>2</sup>, the predictability and statistical validity of model (<italic>Q</italic><sup>2</sup> > 0.5 is considered significant).</p></fn></table-wrap-foot></table-wrap><table-wrap id="t3-ijms-14-12533" position="float"><label>Table 3</label><caption><p>The VIP (variable importance in the projections) values of the major metabolites change in <italic>Rhodococcus fascians</italic>-infected tobacco (LG) contributing for the separation in the OPLS-DA score plots.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="bottom" rowspan="1" colspan="1">Significant polar metabolites</th><th align="center" valign="bottom" rowspan="1" colspan="1"><sup>1</sup>H chemical shifts (ppm)</th><th align="center" valign="bottom" rowspan="1" colspan="1">VIP values</th></tr></thead><tbody><tr><td align="center" valign="top" rowspan="1" colspan="1">5,<italic>O</italic>-caffeoylquinic acid</td><td align="center" valign="top" rowspan="1" colspan="1">3.73 (dd, <italic>J</italic> = 9.7 Hz, 3.5 Hz, H-4)</td><td align="center" valign="top" rowspan="1" colspan="1">6.48</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">Inositol</td><td align="center" valign="top" rowspan="1" colspan="1">3.61 (t, <italic>J</italic> = 9.7 Hz, H-4 and 6)</td><td align="center" valign="top" rowspan="1" colspan="1">4.94</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">Proline</td><td align="center" valign="top" rowspan="1" colspan="1">2.34 (m, H-3)</td><td align="center" valign="top" rowspan="1" colspan="1">4.61</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">Malic acid</td><td align="center" valign="top" rowspan="1" colspan="1">2.80 (dd, <italic>J</italic> = 15.9 Hz, 4.5 Hz, H-<italic>b</italic>)</td><td align="center" valign="top" rowspan="1" colspan="1">2.33</td></tr></tbody></table></table-wrap><table-wrap id="t4-ijms-14-12533" position="float"><label>Table 4</label><caption><p>Determination of <italic>in vitro</italic> growth activity of LG and NI tobacco crude extracts.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" rowspan="3" colspan="1">Cell lines</th><th colspan="4" align="center" valign="bottom" rowspan="1">Infected plants (IC<sub>50</sub> μg/mL)</th><th colspan="4" align="center" valign="bottom" rowspan="1">Non infected plants (IC<sub>50</sub> μg/mL)</th></tr><tr><th colspan="4" align="left" valign="bottom" rowspan="1"><hr></hr></th><th colspan="4" align="left" valign="bottom" rowspan="1"><hr></hr></th></tr><tr><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Water</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Methanol</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Chloroform</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Hexan</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Water</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Methanol</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Chloroform</italic></th><th align="center" valign="bottom" rowspan="1" colspan="1"><italic>Hexan</italic></th></tr></thead><tbody><tr><td align="center" valign="top" rowspan="1" colspan="1">A549</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">69.8 ± 0.9</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">MCF-7</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">85.6 ± 1.0</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">PC3</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">84.5 ± 4.3</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td></tr><tr><td align="center" valign="top" rowspan="1" colspan="1">U373</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">58.9 ± 2.0</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">NA</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td><td align="center" valign="top" rowspan="1" colspan="1">>100</td></tr></tbody></table><table-wrap-foot><fn id="tfn3-ijms-14-12533"><p>NA indicates non active fraction.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list></list><tree><noCountry><name sortKey="De Lorenzi, Manuella" sort="De Lorenzi, Manuella" uniqKey="De Lorenzi M" first="Manuella" last="De Lorenzi">Manuella De Lorenzi</name><name sortKey="Duez, Pierre" sort="Duez, Pierre" uniqKey="Duez P" first="Pierre" last="Duez">Pierre Duez</name><name sortKey="El Jaziri, Mondher" sort="El Jaziri, Mondher" uniqKey="El Jaziri M" first="Mondher" last="El Jaziri">Mondher El Jaziri</name><name sortKey="Nacoulma, Aminata P" sort="Nacoulma, Aminata P" uniqKey="Nacoulma A" first="Aminata P." last="Nacoulma">Aminata P. 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