Fungal endophytes of Catharanthus roseus enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis
Identifieur interne : 000171 ( Pmc/Checkpoint ); précédent : 000170; suivant : 000172Fungal endophytes of Catharanthus roseus enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis
Auteurs : Shiv S. Pandey [Inde] ; Sucheta Singh [Inde] ; C. S. Vivek Babu ; Karuna Shanker [Inde] ; N. K. Srivastava [Inde] ; Ashutosh K. Shukla [Inde] ; Alok Kalra [Inde]Source :
- Scientific Reports [ 2045-2322 ] ; 2016.
Abstract
Not much is known about the mechanism of endophyte-mediated induction of secondary metabolite production in
Url:
DOI: 10.1038/srep26583
PubMed: 27220774
PubMed Central: 4879578
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Fungal endophytes of <italic>Catharanthus roseus</italic> enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis</title><author><name sortKey="Pandey, Shiv S" sort="Pandey, Shiv S" uniqKey="Pandey S" first="Shiv S." last="Pandey">Shiv S. Pandey</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Singh, Sucheta" sort="Singh, Sucheta" uniqKey="Singh S" first="Sucheta" last="Singh">Sucheta Singh</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Babu, C S Vivek" sort="Babu, C S Vivek" uniqKey="Babu C" first="C. S. Vivek" last="Babu">C. S. Vivek Babu</name><affiliation><nlm:aff id="a2"><institution>CSIR</institution><country>-Cent</country><institution>ral Institute of Medicinal and Aromatic Plants, Research Centre</institution>, Allalasandra, GKVK Post, Bangalore-560065,<country>India</country></nlm:aff><wicri:noCountry code="nlm country">-Cent</wicri:noCountry></affiliation></author><author><name sortKey="Shanker, Karuna" sort="Shanker, Karuna" uniqKey="Shanker K" first="Karuna" last="Shanker">Karuna Shanker</name><affiliation wicri:level="1"><nlm:aff id="a3"><institution>Analytical Chemistry Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Srivastava, N K" sort="Srivastava, N K" uniqKey="Srivastava N" first="N. K." last="Srivastava">N. K. Srivastava</name><affiliation wicri:level="1"><nlm:aff id="a4"><institution>Plant Physiology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Shukla, Ashutosh K" sort="Shukla, Ashutosh K" uniqKey="Shukla A" first="Ashutosh K." last="Shukla">Ashutosh K. Shukla</name><affiliation wicri:level="1"><nlm:aff id="a5"><institution>Biotechnology Division, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kalra, Alok" sort="Kalra, Alok" uniqKey="Kalra A" first="Alok" last="Kalra">Alok Kalra</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27220774</idno><idno type="pmc">4879578</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4879578</idno><idno type="RBID">PMC:4879578</idno><idno type="doi">10.1038/srep26583</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000466</idno><idno type="wicri:Area/Pmc/Curation">000465</idno><idno type="wicri:Area/Pmc/Checkpoint">000171</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Fungal endophytes of <italic>Catharanthus roseus</italic> enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis</title><author><name sortKey="Pandey, Shiv S" sort="Pandey, Shiv S" uniqKey="Pandey S" first="Shiv S." last="Pandey">Shiv S. Pandey</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Singh, Sucheta" sort="Singh, Sucheta" uniqKey="Singh S" first="Sucheta" last="Singh">Sucheta Singh</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Babu, C S Vivek" sort="Babu, C S Vivek" uniqKey="Babu C" first="C. S. Vivek" last="Babu">C. S. Vivek Babu</name><affiliation><nlm:aff id="a2"><institution>CSIR</institution><country>-Cent</country><institution>ral Institute of Medicinal and Aromatic Plants, Research Centre</institution>, Allalasandra, GKVK Post, Bangalore-560065,<country>India</country></nlm:aff><wicri:noCountry code="nlm country">-Cent</wicri:noCountry></affiliation></author><author><name sortKey="Shanker, Karuna" sort="Shanker, Karuna" uniqKey="Shanker K" first="Karuna" last="Shanker">Karuna Shanker</name><affiliation wicri:level="1"><nlm:aff id="a3"><institution>Analytical Chemistry Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Srivastava, N K" sort="Srivastava, N K" uniqKey="Srivastava N" first="N. K." last="Srivastava">N. K. Srivastava</name><affiliation wicri:level="1"><nlm:aff id="a4"><institution>Plant Physiology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Shukla, Ashutosh K" sort="Shukla, Ashutosh K" uniqKey="Shukla A" first="Ashutosh K." last="Shukla">Ashutosh K. Shukla</name><affiliation wicri:level="1"><nlm:aff id="a5"><institution>Biotechnology Division, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kalra, Alok" sort="Kalra, Alok" uniqKey="Kalra A" first="Alok" last="Kalra">Alok Kalra</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Not much is known about the mechanism of endophyte-mediated induction of secondary metabolite production in <italic>Catharanthus roseus</italic>. In the present study two fungal endophytes, <italic>Curvularia</italic> sp. CATDLF5 and <italic>Choanephora infundibulifera</italic> CATDLF6 were isolated from the leaves of the plant that were found to enhance vindoline content by 229–403%. The isolated endophytes did not affect the primary metabolism of the plant as the maximum quantum efficiency of PSII, net CO<sub>2</sub> assimilation, plant biomass and starch content of endophyte-inoculated plants was similar to endophyte-free control plants. Expression of terpenoid indole alkaloid (TIA) pathway genes, geraniol 10-hydroxylase (<italic>G10H</italic>), tryptophan decarboxylase (<italic>TDC</italic>), strictosidine synthase (<italic>STR</italic>), 16-hydoxytabersonine-<italic>O</italic>-methyltransferase (<italic>16OMT</italic>), desacetoxyvindoline-4-hydroxylase (<italic>D4H</italic>), deacetylvindoline-4-<italic>O</italic>-acetyltransferase (<italic>DAT</italic>) were upregulated in endophyte-inoculated plants. Endophyte inoculation upregulated the expression of the gene for transcriptional activator octadecanoid-responsive Catharanthus AP2-domain protein (<italic>ORCA3</italic>) and downregulated the expression of Cys2/His2-type zinc finger protein family transcriptional repressors (<italic>ZCTs</italic>). The gene for the vacuolar class III peroxidase (<italic>PRX1</italic>), responsible for coupling vindoline and catharanthine, was upregulated in endophyte-inoculated plants. These endophytes may enhance vindoline production by modulating the expression of key structural and regulatory genes of vindoline biosynthesis without affecting the primary metabolism of the host plant.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Kusari, S" uniqKey="Kusari S">S. Kusari</name></author><author><name sortKey="Hertweck, C" uniqKey="Hertweck C">C. Hertweck</name></author><author><name sortKey="Spiteller, M" uniqKey="Spiteller M">M. 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<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">27220774</article-id><article-id pub-id-type="pmc">4879578</article-id><article-id pub-id-type="pii">srep26583</article-id><article-id pub-id-type="doi">10.1038/srep26583</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Fungal endophytes of <italic>Catharanthus roseus</italic> enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Pandey</surname><given-names>Shiv S.</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>Singh</surname><given-names>Sucheta</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>Babu</surname><given-names>C. S. Vivek</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Shanker</surname><given-names>Karuna</given-names></name><xref ref-type="aff" rid="a3">3</xref></contrib><contrib contrib-type="author"><name><surname>Srivastava</surname><given-names>N. K.</given-names></name><xref ref-type="aff" rid="a4">4</xref></contrib><contrib contrib-type="author"><name><surname>Shukla</surname><given-names>Ashutosh K.</given-names></name><xref ref-type="aff" rid="a5">5</xref></contrib><contrib contrib-type="author"><name><surname>Kalra</surname><given-names>Alok</given-names></name><xref ref-type="corresp" rid="c2">b</xref><xref ref-type="aff" rid="a1">1</xref></contrib><aff id="a1"><label>1</label><institution>Microbial Technology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></aff><aff id="a2"><label>2</label><institution>CSIR</institution><country>-Cent</country><institution>ral Institute of Medicinal and Aromatic Plants, Research Centre</institution>, Allalasandra, GKVK Post, Bangalore-560065,<country>India</country></aff><aff id="a3"><label>3</label><institution>Analytical Chemistry Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></aff><aff id="a4"><label>4</label><institution>Plant Physiology Department, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></aff><aff id="a5"><label>5</label><institution>Biotechnology Division, CSIR-Central Institute of Medicinal and Aromatic Plants</institution>, Lucknow-226015,<country>India</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>vivekbabu.cs@cimap.res.in</email></corresp><corresp id="c2"><label>b</label><email>alok.kalra@yahoo.com</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>25</day><month>05</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>6</volume><elocation-id>26583</elocation-id><history><date date-type="received"><day>11</day><month>11</month><year>2015</year></date><date date-type="accepted"><day>13</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>Not much is known about the mechanism of endophyte-mediated induction of secondary metabolite production in <italic>Catharanthus roseus</italic>. In the present study two fungal endophytes, <italic>Curvularia</italic> sp. CATDLF5 and <italic>Choanephora infundibulifera</italic> CATDLF6 were isolated from the leaves of the plant that were found to enhance vindoline content by 229–403%. The isolated endophytes did not affect the primary metabolism of the plant as the maximum quantum efficiency of PSII, net CO<sub>2</sub> assimilation, plant biomass and starch content of endophyte-inoculated plants was similar to endophyte-free control plants. Expression of terpenoid indole alkaloid (TIA) pathway genes, geraniol 10-hydroxylase (<italic>G10H</italic>), tryptophan decarboxylase (<italic>TDC</italic>), strictosidine synthase (<italic>STR</italic>), 16-hydoxytabersonine-<italic>O</italic>-methyltransferase (<italic>16OMT</italic>), desacetoxyvindoline-4-hydroxylase (<italic>D4H</italic>), deacetylvindoline-4-<italic>O</italic>-acetyltransferase (<italic>DAT</italic>) were upregulated in endophyte-inoculated plants. Endophyte inoculation upregulated the expression of the gene for transcriptional activator octadecanoid-responsive Catharanthus AP2-domain protein (<italic>ORCA3</italic>) and downregulated the expression of Cys2/His2-type zinc finger protein family transcriptional repressors (<italic>ZCTs</italic>). The gene for the vacuolar class III peroxidase (<italic>PRX1</italic>), responsible for coupling vindoline and catharanthine, was upregulated in endophyte-inoculated plants. These endophytes may enhance vindoline production by modulating the expression of key structural and regulatory genes of vindoline biosynthesis without affecting the primary metabolism of the host plant.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Schematic representation of the terpenoid indole alkaloid (TIA) biosynthetic pathway.</title><p><italic>Enzyme abbreviations:</italic> DXS, 1-deoxy-D-xylulose-5-phosphate synthase; IPP, isopentenyl pyrophosphate; DMAPP, dimethylallyl pyrophosphate; IDI1, isopentenyl diphosphate isomerase 1; CPR, cytochrome P450 reductase; G10H, geraniol 10-hydroxylase; UGT8, UDP-sugar glucosyltransferase 8, 7-DLH, 7-deoxyloganic acid hydroxylase; LAMT, loganic acid <italic>O</italic>-methyltransferase; SLS, secologanin synthase; AS, anthranilate synthase; TDC, tryptophan decarboxylase; STR, strictosidine synthase; SGD, strictosidine glucosidase; T16H, tabersonine 16-hydroxylase; 16OMT, 16-hydoxytabersonine-<italic>O</italic>-methyltransferase; NMT, <italic>N</italic>-methyltransferase; D4H, desacetoxyvindoline-4-hydroxylase; DAT, deacetylvindoline-4-<italic>O</italic>-acetyltransferase; and PRX, vacuolar class III peroxidase.</p></caption><graphic xlink:href="srep26583-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Fungal endophytes isolated from <italic>Catharanthus roseus</italic> and their effect on vindoline content in plant leaves.</title><p>Upper panel: Fungal endophytes isolated from the surface sterilized leaves of <italic>C. roseus</italic> (cv. Dhawal) plants. Surface sterilized leaves were cut into small pieces and kept on potato dextrose agar plate, whereby endophytes were found to originate from the margin of the pieces (inset picture). Lower panel: Endophyte-free <italic>C. roseus</italic> (cv. Prabal) plants (generated from seeds treated with bactericide and fungicide) were used to study the effect of treatment with endophytes (CATDLF5 and CATDLF6 isolated from cv. Dhawal) on leaf vindoline content. Two types of controls were included in the study-(i) the endophyte-free control [C] plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte and (ii) the natural control [NC] plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants. Fungal endophyte inoculums (1 × 10<sup>8</sup> spore/conidia mL<sup>−1</sup>) prepared in phosphate buffer saline (PBS) were used to treat roots of experimental plants. The roots of both the controls–endophyte-free (C) and natural (NC) plants were treated with PBS. Third leaves of 90 d-old plants were sampled for vindoline content (% dry weight basis). As biological replicates, three plants per treatment were analyzed. For each biological replicate, three technical replicates were run on the HPLC and the mean of the three technical replicates represented the particular biological replicate. Statistical analysis was carried out for the data obtained for the three biological replicates (n = 3). Asterisks indicate significant differences as compared to the endophyte-free control (C) (Duncan’s multiple range test *<italic>P</italic> < 0.05).</p></caption><graphic xlink:href="srep26583-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Effect of endophytes (CATDLF5 and CATDLF6) on expression of genes involved in secologanin and tryptamine biosynthesis.</title><p>Transcript abundance of (<bold>a</bold>) <italic>DXS</italic>, (<bold>b</bold>) <italic>CPR</italic>, (<bold>c</bold>) <italic>G10H</italic>, (<bold>d</bold>) <italic>UGT8</italic>, (<bold>e</bold>) <italic>LAMT</italic>, (<bold>f</bold>) <italic>SLS</italic>, (<bold>g</bold>) <italic>AS</italic>, (<bold>h</bold>) <italic>TDC</italic> was analyzed. NC- the natural control plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants. C- the endophyte-free control plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte. The endophyte-free control (C) was used as the calibrator. For normalization, <italic>C. roseus</italic> actin gene was used as the endogenous gene. Data are means ± SD (<italic>n</italic> = 3 biological replicates) and <italic>Y</italic>-axis represents relative quantity (RQ). Asterisks indicate significant differences as compared to the endophyte-free control (C) (Duncan’s multiple range test *<italic>P</italic> < 0.05).</p></caption><graphic xlink:href="srep26583-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>Effect of endophytes (CATDLF5 and CATDLF6) on expression of genes involved in vindoline biosynthesis.</title><p>Transcript abundance of (<bold>a</bold>) <italic>STR</italic>, (<bold>b</bold>) <italic>SGD</italic>, (<bold>c</bold>) <italic>T16H</italic>, (<bold>d</bold>) <italic>16OMT</italic>, (<bold>e</bold>) <italic>D4H</italic>, (<bold>f</bold>) <italic>DAT</italic> was analyzed. NC- the natural control plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants. C- the endophyte-free control plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte. The endophyte-free control (C) was used as the calibrator. For normalization, <italic>C. roseus</italic> actin gene was used as the endogenous gene. Data are means ± SD (<italic>n</italic> = 3 biological replicates) and <italic>Y</italic>-axis represents relative quantity (RQ). Asterisks indicate significant differences as compared to the endophyte-free control (C) (Duncan’s multiple range test *<italic>P</italic> < 0.05).</p></caption><graphic xlink:href="srep26583-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>Effect of endophytes (CATDLF5 and CATDLF6) on <italic>PRX1</italic> expression and hydrogen peroxide concentration.</title><p>(<bold>a</bold>) Transcript abundance of <italic>PRX1</italic>, (<bold>b</bold>) Hydrogen peroxide concentration in the plant leaf. NC- the natural control plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants. C- the endophyte-free control plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte. In the qRT-PCR analysis, the endophyte-free control (C) was used as the calibrator and for normalization, <italic>C. roseus</italic> actin gene was used as the endogenous gene. In (<bold>a</bold>) <italic>Y</italic>-axis represents relative quantity (RQ). Data are means ± SD (<italic>n</italic> = 3 biological replicates). Values with different letters are significantly different (Duncan’s multiple range test *<italic>P</italic> < 0.05).</p></caption><graphic xlink:href="srep26583-f5"></graphic></fig><fig id="f6"><label>Figure 6</label><caption><title>Effect of endophytes (CATDLF5 and CATDLF6) on expression of transcriptional activators.</title><p>Transcript abundance of (<bold>a</bold>) <italic>ORCA2</italic>, (<bold>b</bold>) <italic>ORCA3</italic>, (<bold>c</bold>) <italic>BPF1</italic>, (<bold>d</bold>) <italic>MYC2</italic> was analyzed. NC- the natural control plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants. C- the endophyte-free control plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte. The endophyte-free control (C) was used as the calibrator. For normalization, <italic>C. roseus</italic> actin gene was used as the endogenous gene. Data are means ± SD (<italic>n</italic> = 3 biological replicates) and <italic>Y</italic>-axis represents relative quantity (RQ). Asterisks indicate significant differences as compared to the endophyte-free control (C) (Duncan’s multiple range test *<italic>P</italic> < 0.05).</p></caption><graphic xlink:href="srep26583-f6"></graphic></fig><fig id="f7"><label>Figure 7</label><caption><title>Effect of endophytes (CATDLF5 and CATDLF6) on expression of transcriptional repressors and mitogen activated protein kinase 3.</title><p>Transcript abundance of (<bold>a</bold>) <italic>ZCT1</italic>, (<bold>b</bold>) <italic>ZCT2</italic>, (<bold>c</bold>) <italic>ZCT3</italic>, (<bold>d</bold>) <italic>GBF1</italic>, (<bold>e</bold>) <italic>GBF2</italic>, (<bold>f</bold>) <italic>MPK3</italic> was analyzed. NC- the natural control plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants. C- the endophyte-free control plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte. The endophyte-free control (C) was used as the calibrator. For normalization actin gene was used as the endogenous gene. Data are means ± SD (<italic>n</italic> = 3 biological replicates) and <italic>Y</italic>-axis represents relative quantity (RQ). Asterisks indicate significant differences as compared to the endophyte-free control (C) (Duncan’s multiple range test *<italic>P</italic> < 0.05).</p></caption><graphic xlink:href="srep26583-f7"></graphic></fig><table-wrap position="float" id="t1"><label>Table 1</label><caption><title>Effect of inoculation with endophytes (CATDLF5 and CATDLF6) on physiological and growth parameters of <italic>Catharanthus roseus</italic> plants.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center" char="±"></col><col align="center" char="±"></col><col align="center" char="±"></col><col align="center" char="±"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">Treatment</th><th align="center" valign="top" char="±" charoff="50">NC</th><th align="center" valign="top" char="±" charoff="50">C</th><th align="center" valign="top" char="±" charoff="50">CATDLF5</th><th align="center" valign="top" char="±" charoff="50">CATDLF6</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Chlorophyll (mg gFW<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">1.74 ± 0.03<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">1.55 ± 0.03<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">1.61 ± 0.04<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">1.55 ± 0.03<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Carotenoids (mg gFW<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">0.07 ± 0.010<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">0.06 ± 0.005<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">0.06 ± 0.003<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">0.07 ± 0.004<sup>a</sup></td></tr><tr><td align="left" valign="top" charoff="50">Fv/Fm</td><td align="center" valign="top" char="±" charoff="50">0.83 ± 0.01<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">0.73 ± 0.01<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">0.73 ± 0.02<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">0.75 ± 0.02<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">A (μmol m<sup>−2</sup> s<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">14.77 ± 0.43<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">11.97 ± 0.20<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">12.47 ± 0.60<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">11.70 ± 0.71<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">E (mmol m<sup>−2</sup> s<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">10.63 ± 0.46<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">8.59 ± 0.41<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">8.91 ± 0.17<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">8.81 ± 0.44<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">gS (mmol m<sup>−2</sup> s<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">481.00 ± 5.13<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">432.00 ± 8.02<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">432.33 ± 12.12<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">410.70 ± 10.68<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Starch (mmol m<sup>−2</sup>)</td><td align="center" valign="top" char="±" charoff="50">41.35 ± 0.56<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">32.45 ± 1.43<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">32.19 ± 3.42<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">30.54 ± 2.04<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Biomass (g Plant<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">5.03 ± 0.40<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">3.23 ± 0.22<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">3.14 ± 0.10<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">3.27 ± 0.23<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Number of leaves (Plant<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">75.33 ± 2.90<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">58.67 ± 3.52<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">59.33 ± 4.37<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">55.00 ± 2.60<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Number of siliques (Plant<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">23.00 ± 1.15<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">16.00 ± 1.15<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">17.33 ± 1.20<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">15.67 ± 1.45<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Number of branches (Plant<sup>−1</sup>)</td><td align="center" valign="top" char="±" charoff="50">5.67 ± 0.27<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">4.33 ± 0.27<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">4.33 ± 0.13<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">4.67 ± 0.13<sup>b</sup></td></tr><tr><td align="left" valign="top" charoff="50">Plant height (cm)</td><td align="center" valign="top" char="±" charoff="50">39.67 ± 1.20<sup>a</sup></td><td align="center" valign="top" char="±" charoff="50">35.67 ± 0.33<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">36.00 ± 1.31<sup>b</sup></td><td align="center" valign="top" char="±" charoff="50">33.33 ± 2.40<sup>b</sup></td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p>NC- the natural control plants that originated from <italic>C. roseus</italic> seeds that were not treated with any bacteriocide and fungicide and contained all the naturally occurring endophytes present in the plants.</p></fn><fn id="t1-fn2"><p>C- the endophyte-free control plants that originated from <italic>C. roseus</italic> seeds treated with bactericides and fungicides and were thus devoid of any naturally occurring endophyte. Fv/Fm indicates the quantum efficiency of photosynthesis, A-Net CO<sub>2</sub> assimilation, E-Transpiration rate, gS-Stomatal conductance.</p></fn><fn id="t1-fn3"><p>Values are the means of six biological replicates ± S.E. Values with different letters (a, b) are significantly different at <italic>P</italic> ≤ 0.05 (Duncan’s multiple range test).</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>Inde</li></country></list><tree><noCountry><name sortKey="Babu, C S Vivek" sort="Babu, C S Vivek" uniqKey="Babu C" first="C. S. Vivek" last="Babu">C. S. Vivek Babu</name></noCountry><country name="Inde"><noRegion><name sortKey="Pandey, Shiv S" sort="Pandey, Shiv S" uniqKey="Pandey S" first="Shiv S." last="Pandey">Shiv S. Pandey</name></noRegion><name sortKey="Kalra, Alok" sort="Kalra, Alok" uniqKey="Kalra A" first="Alok" last="Kalra">Alok Kalra</name><name sortKey="Shanker, Karuna" sort="Shanker, Karuna" uniqKey="Shanker K" first="Karuna" last="Shanker">Karuna Shanker</name><name sortKey="Shukla, Ashutosh K" sort="Shukla, Ashutosh K" uniqKey="Shukla A" first="Ashutosh K." last="Shukla">Ashutosh K. Shukla</name><name sortKey="Singh, Sucheta" sort="Singh, Sucheta" uniqKey="Singh S" first="Sucheta" last="Singh">Sucheta Singh</name><name sortKey="Srivastava, N K" sort="Srivastava, N K" uniqKey="Srivastava N" first="N. K." last="Srivastava">N. K. Srivastava</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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