Analysis of Synonymous Codon Usage Patterns in Seven Different Citrus Species
Identifieur interne : 000F02 ( Pmc/Curation ); précédent : 000F01; suivant : 000F03Analysis of Synonymous Codon Usage Patterns in Seven Different Citrus Species
Auteurs : Chen Xu [République populaire de Chine] ; Jing Dong [République populaire de Chine] ; Chunfa Tong [République populaire de Chine] ; Xindong Gong [République populaire de Chine] ; Qiang Wen [République populaire de Chine] ; Qiang Zhuge [République populaire de Chine]Source :
- Evolutionary Bioinformatics Online [ 1176-9343 ] ; 2013.
Abstract
We used large samples of expressed sequence tags to characterize the patterns of codon usage bias (CUB) in seven different
Url:
DOI: 10.4137/EBO.S11930
PubMed: 23761955
PubMed Central: 3667683
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Analysis of Synonymous Codon Usage Patterns in Seven Different <italic>Citrus</italic> Species</title><author><name sortKey="Xu, Chen" sort="Xu, Chen" uniqKey="Xu C" first="Chen" last="Xu">Chen Xu</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-ebo-9-2013-215">Biology Department, Nanjing Xiaozhuang University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Biology Department, Nanjing Xiaozhuang University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Dong, Jing" sort="Dong, Jing" uniqKey="Dong J" first="Jing" last="Dong">Jing Dong</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Tong, Chunfa" sort="Tong, Chunfa" uniqKey="Tong C" first="Chunfa" last="Tong">Chunfa Tong</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Gong, Xindong" sort="Gong, Xindong" uniqKey="Gong X" first="Xindong" last="Gong">Xindong Gong</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Wen, Qiang" sort="Wen, Qiang" uniqKey="Wen Q" first="Qiang" last="Wen">Qiang Wen</name><affiliation wicri:level="1"><nlm:aff id="af3-ebo-9-2013-215">Jiangxi Forestry Academy, Nanchang, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Jiangxi Forestry Academy, Nanchang</wicri:regionArea></affiliation></author><author><name sortKey="Zhuge, Qiang" sort="Zhuge, Qiang" uniqKey="Zhuge Q" first="Qiang" last="Zhuge">Qiang Zhuge</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23761955</idno><idno type="pmc">3667683</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3667683</idno><idno type="RBID">PMC:3667683</idno><idno type="doi">10.4137/EBO.S11930</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">000F03</idno><idno type="wicri:Area/Pmc/Curation">000F02</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Analysis of Synonymous Codon Usage Patterns in Seven Different <italic>Citrus</italic> Species</title><author><name sortKey="Xu, Chen" sort="Xu, Chen" uniqKey="Xu C" first="Chen" last="Xu">Chen Xu</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-ebo-9-2013-215">Biology Department, Nanjing Xiaozhuang University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Biology Department, Nanjing Xiaozhuang University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Dong, Jing" sort="Dong, Jing" uniqKey="Dong J" first="Jing" last="Dong">Jing Dong</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Tong, Chunfa" sort="Tong, Chunfa" uniqKey="Tong C" first="Chunfa" last="Tong">Chunfa Tong</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Gong, Xindong" sort="Gong, Xindong" uniqKey="Gong X" first="Xindong" last="Gong">Xindong Gong</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author><author><name sortKey="Wen, Qiang" sort="Wen, Qiang" uniqKey="Wen Q" first="Qiang" last="Wen">Qiang Wen</name><affiliation wicri:level="1"><nlm:aff id="af3-ebo-9-2013-215">Jiangxi Forestry Academy, Nanchang, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>Jiangxi Forestry Academy, Nanchang</wicri:regionArea></affiliation></author><author><name sortKey="Zhuge, Qiang" sort="Zhuge, Qiang" uniqKey="Zhuge Q" first="Qiang" last="Zhuge">Qiang Zhuge</name><affiliation wicri:level="1"><nlm:aff id="af1-ebo-9-2013-215">The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</nlm:aff><country xml:lang="fr" wicri:curation="lc">République populaire de Chine</country><wicri:regionArea>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing</wicri:regionArea></affiliation></author></analytic><series><title level="j">Evolutionary Bioinformatics Online</title><idno type="eISSN">1176-9343</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>We used large samples of expressed sequence tags to characterize the patterns of codon usage bias (CUB) in seven different <italic>Citrus</italic> species and to analyze their evolutionary effect on selection and base composition. We found that A- and T-ending codons are predominant in <italic>Citrus</italic> species. Next, we identified 21 codons for 18 different amino acids that were considered preferred codons in all seven species. We then performed correspondence analysis and constructed plots for the effective number of codons (ENCs) to analyze synonymous codon usage. Multiple regression analysis showed that gene expression in each species had a constant influence on the frequency of optional codons (FOP). Base composition differences between the proportions were large. Finally, positive selection was detected during the evolutionary process of the different <italic>Citrus</italic> species. Overall, our results suggest that codon usages were the result of positive selection. Codon usage variation among <italic>Citrus</italic> genes is influenced by translational selection, mutational bias, and gene length. CUB is strongly affected by selection pressure at the translational level, and gene length plays only a minor role. One possible explanation for this is that the selection-mediated codon bias is consistently strong in <italic>Citrus</italic>, which is one of the most widely cultivated fruit trees.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Plotkin, Jb" uniqKey="Plotkin J">JB Plotkin</name></author><author><name sortKey="Kudla, G" uniqKey="Kudla G">G Kudla</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Plotkin, Jb" uniqKey="Plotkin J">JB Plotkin</name></author><author><name sortKey="Dushoff, J" uniqKey="Dushoff J">J Dushoff</name></author><author><name sortKey="Desai, Mm" uniqKey="Desai M">MM Desai</name></author><author><name sortKey="Fraser, Hb" uniqKey="Fraser H">HB Fraser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Camiolo, S" uniqKey="Camiolo S">S Camiolo</name></author><author><name sortKey="Farina, L" uniqKey="Farina L">L Farina</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Evol Bioinform Online</journal-id><journal-id journal-id-type="iso-abbrev">Evol. Bioinform. Online</journal-id><journal-id journal-id-type="publisher-id">101256319</journal-id><journal-title-group><journal-title>Evolutionary Bioinformatics Online</journal-title></journal-title-group><issn pub-type="epub">1176-9343</issn><publisher><publisher-name>Libertas Academica</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23761955</article-id><article-id pub-id-type="pmc">3667683</article-id><article-id pub-id-type="doi">10.4137/EBO.S11930</article-id><article-id pub-id-type="publisher-id">ebo-9-2013-215</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Research</subject></subj-group></article-categories><title-group><article-title>Analysis of Synonymous Codon Usage Patterns in Seven Different <italic>Citrus</italic> Species</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Xu</surname><given-names>Chen</given-names></name><xref ref-type="aff" rid="af1-ebo-9-2013-215"><sup>1</sup></xref><xref ref-type="aff" rid="af2-ebo-9-2013-215"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dong</surname><given-names>Jing</given-names></name><xref ref-type="aff" rid="af1-ebo-9-2013-215"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tong</surname><given-names>Chunfa</given-names></name><xref ref-type="aff" rid="af1-ebo-9-2013-215"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gong</surname><given-names>Xindong</given-names></name><xref ref-type="aff" rid="af1-ebo-9-2013-215"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wen</surname><given-names>Qiang</given-names></name><xref ref-type="aff" rid="af3-ebo-9-2013-215"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhuge</surname><given-names>Qiang</given-names></name><xref ref-type="aff" rid="af1-ebo-9-2013-215"><sup>1</sup></xref><xref ref-type="corresp" rid="c1-ebo-9-2013-215"></xref></contrib></contrib-group><aff id="af1-ebo-9-2013-215"><label>1</label>The Key Lab of Forest Genetics and Gene Engineering, Nanjing Forestry University, Nanjing, China.</aff><aff id="af2-ebo-9-2013-215"><label>2</label>Biology Department, Nanjing Xiaozhuang University, Nanjing, China.</aff><aff id="af3-ebo-9-2013-215"><label>3</label>Jiangxi Forestry Academy, Nanchang, China.</aff><author-notes><corresp id="c1-ebo-9-2013-215">Corresponding author email: <email>qzhuge@njfu.edu.cn</email></corresp></author-notes><pub-date pub-type="collection"><year>2013</year></pub-date><pub-date pub-type="epub"><day>23</day><month>5</month><year>2013</year></pub-date><volume>9</volume><fpage>215</fpage><lpage>228</lpage><permissions><copyright-statement>© 2013 the author(s), publisher and licensee Libertas Academica Ltd.</copyright-statement><copyright-year>2013</copyright-year><license license-type="open-access"><license-p>This is an open access article published under the Creative Commons CC-BY-NC 3.0 license.</license-p></license></permissions><abstract><p>We used large samples of expressed sequence tags to characterize the patterns of codon usage bias (CUB) in seven different <italic>Citrus</italic> species and to analyze their evolutionary effect on selection and base composition. We found that A- and T-ending codons are predominant in <italic>Citrus</italic> species. Next, we identified 21 codons for 18 different amino acids that were considered preferred codons in all seven species. We then performed correspondence analysis and constructed plots for the effective number of codons (ENCs) to analyze synonymous codon usage. Multiple regression analysis showed that gene expression in each species had a constant influence on the frequency of optional codons (FOP). Base composition differences between the proportions were large. Finally, positive selection was detected during the evolutionary process of the different <italic>Citrus</italic> species. Overall, our results suggest that codon usages were the result of positive selection. Codon usage variation among <italic>Citrus</italic> genes is influenced by translational selection, mutational bias, and gene length. CUB is strongly affected by selection pressure at the translational level, and gene length plays only a minor role. One possible explanation for this is that the selection-mediated codon bias is consistently strong in <italic>Citrus</italic>, which is one of the most widely cultivated fruit trees.</p></abstract><kwd-group><kwd>citrus</kwd><kwd>codon usage</kwd><kwd>evolution</kwd></kwd-group></article-meta></front><floats-group><fig id="f1-ebo-9-2013-215" position="float"><label>Figure 1</label><caption><p>Effective number of codons (ENC) as a measure of overall average codon usage bias (CUB) in seven <italic>Citrus</italic> species. The actual mean ENC, mean GC3s, and mean GC are shown below each bar. 95% confidence bars in standard error of mean are shown. A lower ENC represents greater bias.</p></caption><graphic xlink:href="ebo-9-2013-215f1"></graphic></fig><fig id="f2-ebo-9-2013-215" position="float"><label>Figure 2</label><caption><p>The ENC plot of <italic>Citrus</italic>. The continuous curve represents the relationship between GC3s and ENC values under random codon usage.</p></caption><graphic xlink:href="ebo-9-2013-215f2"></graphic></fig><fig id="f3-ebo-9-2013-215" position="float"><label>Figure 3</label><caption><p>Proportion of variation in the frequency of optimal codon usage explained by gene expression, gene length, and base composition at synonymous sites.</p></caption><graphic xlink:href="ebo-9-2013-215f3"></graphic></fig><fig id="f4-ebo-9-2013-215" position="float"><label>Figure 4</label><caption><p>Prediction of the ω value of each branch during evolutionary processes. Unrooted tree representing the phylogenetic relationship between the seven species. ML estimates non-synonymous (dN) and synonymous (dS) substitution rates, dN/dS ratios (in parentheses), and the maximum likelihood estimates of selection acting on preferred codons are shown above each branch and are calculated from the concatenated data set of 84 genes. Branch lengths are proportional to the synonymous substitution rate.</p></caption><graphic xlink:href="ebo-9-2013-215f4"></graphic></fig><table-wrap id="t1-ebo-9-2013-215" position="float"><label>Table 1</label><caption><p>Differences in relative synonymous codon usage (RSCU) across codons between genes with high and low levels of expression.</p></caption><graphic xlink:href="ebo-9-2013-215t1"></graphic><table-wrap-foot><fn id="tfn1-ebo-9-2013-215"><p><bold>Notes:</bold> The right-most column shows codons with significantly increased usage in highly expressed genes, as determined by a <italic>t</italic>-test (<italic>P</italic> < 0.05). Each * represents a species for which the <italic>t</italic>-test was significant, in the order as they are listed in the figure. Codons above the horizontal dotted lines were used to design the optimal codons and were used to calculate frequencies of optimal codon usage (FOP) in all species. The color in the figure indicates the gradient of ΔRSCU values, from the most positive (green) to the most negative (orange).</p></fn></table-wrap-foot></table-wrap><table-wrap id="t2-ebo-9-2013-215" position="float"><label>Table 2</label><caption><p>Optimal codon table in <italic>Citrus sinensis</italic>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="top" rowspan="2" colspan="1"><bold>Amino acid</bold></th><th align="left" valign="top" rowspan="2" colspan="1"><bold>Codon</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>ΔRSCU</bold><hr></hr></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>Frequency per thousand bases</bold><hr></hr></th></tr><tr><th align="left" valign="top" rowspan="1" colspan="1"><bold>From EST</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>From CDS</bold></th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="4" colspan="1">Ala</td><td align="left" valign="top" rowspan="1" colspan="1">GCU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.59</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">29.3</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GCA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.75</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">20.6</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GCC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.81</td><td align="left" valign="top" rowspan="1" colspan="1">15.9</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GCG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.52</td><td align="left" valign="top" rowspan="1" colspan="1">8.3</td></tr><tr><td align="left" valign="top" rowspan="6" colspan="1">Arg</td><td align="left" valign="top" rowspan="1" colspan="1">AGA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.81</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">14.9</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AGG</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.26</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">14.9</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CGU</td><td align="left" valign="top" rowspan="1" colspan="1">−0.02</td><td align="left" valign="top" rowspan="1" colspan="1">5.5</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CGA</td><td align="left" valign="top" rowspan="1" colspan="1">0.09</td><td align="left" valign="top" rowspan="1" colspan="1">4.8</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CGG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.32</td><td align="left" valign="top" rowspan="1" colspan="1">4.4</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CGC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.8</td><td align="left" valign="top" rowspan="1" colspan="1">4.6</td></tr><tr><td align="left" valign="top" rowspan="4" colspan="1">Gly</td><td align="left" valign="top" rowspan="1" colspan="1">GGU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.46</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">19.7</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GGA</td><td align="left" valign="top" rowspan="1" colspan="1">0.37</td><td align="left" valign="top" rowspan="1" colspan="1">18.7</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GGG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.12</td><td align="left" valign="top" rowspan="1" colspan="1">14</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GGC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.71</td><td align="left" valign="top" rowspan="1" colspan="1">17.2</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">His</td><td align="left" valign="top" rowspan="1" colspan="1">CAU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.76</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">12.4</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CAC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.76</td><td align="left" valign="top" rowspan="1" colspan="1">10.6</td></tr><tr><td align="left" valign="top" rowspan="4" colspan="1">Val</td><td align="left" valign="top" rowspan="1" colspan="1">GUU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.59</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">27.6</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GUA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.38</td><td align="left" valign="top" rowspan="1" colspan="1">8.3</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GUC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.66</td><td align="left" valign="top" rowspan="1" colspan="1">11.5</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GUG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.31</td><td align="left" valign="top" rowspan="1" colspan="1">21.2</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Lys</td><td align="left" valign="top" rowspan="1" colspan="1">AAA</td><td align="left" valign="top" rowspan="1" colspan="1">0.17</td><td align="left" valign="top" rowspan="1" colspan="1">25.7</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AAG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.17</td><td align="left" valign="top" rowspan="1" colspan="1">34</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Phe</td><td align="left" valign="top" rowspan="1" colspan="1">UUU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.63</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">23.3</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UUC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.63</td><td align="left" valign="top" rowspan="1" colspan="1">21</td></tr><tr><td align="left" valign="top" rowspan="4" colspan="1">Pro</td><td align="left" valign="top" rowspan="1" colspan="1">CCU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.78</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">16.8</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CCC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.53</td><td align="left" valign="top" rowspan="1" colspan="1">11.2</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CCG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.86</td><td align="left" valign="top" rowspan="1" colspan="1">7.3</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CCA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.61</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">16</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Thr</td><td align="left" valign="top" rowspan="1" colspan="1">ACU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.69</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">18.5</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ACA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.67</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">15.1</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Asn</td><td align="left" valign="top" rowspan="1" colspan="1">AAU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.67</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">24.8</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AAC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.67</td><td align="left" valign="top" rowspan="1" colspan="1">21.7</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Asp</td><td align="left" valign="top" rowspan="1" colspan="1">GAU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.56</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">33.8</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GAC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.56</td><td align="left" valign="top" rowspan="1" colspan="1">18.6</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Cys</td><td align="left" valign="top" rowspan="1" colspan="1">UGU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.52</td><td align="left" valign="top" rowspan="1" colspan="1">8.5</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UGC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.52</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">8.8</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Gln</td><td align="left" valign="top" rowspan="1" colspan="1">CAA</td><td align="left" valign="top" rowspan="1" colspan="1">0.13</td><td align="left" valign="top" rowspan="1" colspan="1">18.7</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CAG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.13</td><td align="left" valign="top" rowspan="1" colspan="1">16.5</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Glu</td><td align="left" valign="top" rowspan="1" colspan="1">GAA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.32</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">28.6</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">GAG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.32</td><td align="left" valign="top" rowspan="1" colspan="1">31.3</td></tr><tr><td align="left" valign="top" rowspan="3" colspan="1">Ile</td><td align="left" valign="top" rowspan="1" colspan="1">AUU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.49</td><td align="left" valign="top" rowspan="1" colspan="1">24.2</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AUA</td><td align="left" valign="top" rowspan="1" colspan="1">0.32</td><td align="left" valign="top" rowspan="1" colspan="1">12.6</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AUC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.81</td><td align="left" valign="top" rowspan="1" colspan="1">16.4</td></tr><tr><td align="left" valign="top" rowspan="6" colspan="1">Leu</td><td align="left" valign="top" rowspan="1" colspan="1">UUA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.48</td><td align="left" valign="top" rowspan="1" colspan="1">12.3</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UUG</td><td align="left" valign="top" rowspan="1" colspan="1">0.25</td><td align="left" valign="top" rowspan="1" colspan="1">22.4</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CUU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.47</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">25.2</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CUA</td><td align="left" valign="top" rowspan="1" colspan="1">0.16</td><td align="left" valign="top" rowspan="1" colspan="1">8.4</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CUC</td><td align="left" valign="top" rowspan="1" colspan="1">−1.24</td><td align="left" valign="top" rowspan="1" colspan="1">14.6</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">CUG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.11</td><td align="left" valign="top" rowspan="1" colspan="1">13</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Met</td><td align="left" valign="top" rowspan="1" colspan="1">AUG</td><td align="left" valign="top" rowspan="1" colspan="1">0</td><td align="left" valign="top" rowspan="1" colspan="1">0</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Tyr</td><td align="left" valign="top" rowspan="1" colspan="1">UAU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.72</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">15.4</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UAC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.72</td><td align="left" valign="top" rowspan="1" colspan="1">13.9</td></tr><tr><td align="left" valign="top" rowspan="6" colspan="1">Ser</td><td align="left" valign="top" rowspan="1" colspan="1">UCU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.7</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">17.7</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UCA</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.52</td><td align="left" valign="top" content-type="background-color:#40AC48" rowspan="1" colspan="1">17</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AGU</td><td align="left" valign="top" content-type="background-color:#D2541E" rowspan="1" colspan="1">0.6</td><td align="left" valign="top" rowspan="1" colspan="1">11.2</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UCC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.81</td><td align="left" valign="top" rowspan="1" colspan="1">9.8</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">UCG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.73</td><td align="left" valign="top" rowspan="1" colspan="1">9.1</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">AGC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.27</td><td align="left" valign="top" rowspan="1" colspan="1">12</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Thr</td><td align="left" valign="top" rowspan="1" colspan="1">ACC</td><td align="left" valign="top" rowspan="1" colspan="1">−0.71</td><td align="left" valign="top" rowspan="1" colspan="1">10.6</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ACG</td><td align="left" valign="top" rowspan="1" colspan="1">−0.66</td><td align="left" valign="top" rowspan="1" colspan="1">6.9</td></tr></tbody></table><table-wrap-foot><fn id="tfn2-ebo-9-2013-215"><p><bold>Notes:</bold> ΔRSCU: Relative synonymous codon usage in predicted genes with high and low gene expression levels based on the EST sequence in <italic>Citrus sinensis</italic>. Optimal codons (red box) were identified based on differences in relative synonymous codon usage. Frequency per thousand bases: use frequency per thousand bases in identified high-confidence coding sequences from full-length cDNA in <italic>Citrus sinensis</italic>. Optimal codons (green box) were identified based on different frequencies per thousand bases (<italic>P</italic> < 0.05).</p></fn></table-wrap-foot></table-wrap><table-wrap id="t3-ebo-9-2013-215" position="float"><label>Table 3</label><caption><p>Parameter estimates and log-likelihood values under models of variable ratios among sites.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="top" rowspan="1" colspan="1"></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>Model</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>P</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>LnL</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>Kappa</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>Estimates of parameters</bold></th><th align="left" valign="top" rowspan="1" colspan="1"><bold>Positively selected sites</bold></th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="4" colspan="1">M1</td><td align="left" valign="top" rowspan="4" colspan="1">Nearly neutral</td><td align="left" valign="top" rowspan="4" colspan="1">1</td><td align="left" valign="top" rowspan="4" colspan="1">−64600.24</td><td align="left" valign="top" rowspan="4" colspan="1">1.55928</td><td align="left" valign="top" rowspan="1" colspan="1">P<sub>0</sub>= 0.20008</td><td align="left" valign="top" rowspan="1" colspan="1">Not allowed</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ω<sub>0</sub>= 0.19552</td><td align="left" valign="top" rowspan="1" colspan="1"></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">P<sub>1</sub>= 0.79992</td><td align="left" valign="top" rowspan="1" colspan="1"></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ω<sub>1</sub>= 1.00000</td><td align="left" valign="top" rowspan="1" colspan="1"></td></tr><tr><td align="left" valign="top" rowspan="14" colspan="1">M2</td><td align="left" valign="top" rowspan="14" colspan="1">Positive selection</td><td align="left" valign="top" rowspan="14" colspan="1">3</td><td align="left" valign="top" rowspan="14" colspan="1">−64282.47</td><td align="left" valign="top" rowspan="14" colspan="1">1.72982</td><td align="left" valign="top" rowspan="1" colspan="1">P<sub>0</sub>= 0.06407</td><td align="left" valign="top" rowspan="1" colspan="1">1Q 5N <bold>9L</bold> 15D 51E 632K 670R 685G 883R 886G 929S</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ω<sub>0</sub>= 0.00000</td><td align="left" valign="top" rowspan="1" colspan="1">1031W 1037A 1353E 1384R 1388S 1394H 1400A 1413D</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">P<sub>1</sub>= 0.77815</td><td align="left" valign="top" rowspan="1" colspan="1">1418L 1737E 1738R 1742C 1760V 1769S 1770R 1787V</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ω<sub>1</sub>= 1.00000</td><td align="left" valign="top" rowspan="1" colspan="1">1973R 1976R 1992A 1995S 2266L 2272N 2280L 2283S</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">P<sub>2</sub>= 0.15778</td><td align="left" valign="top" rowspan="1" colspan="1">2285S <bold>2298V 2304P</bold> 2305F <bold>2308N</bold> 2352R 2362R 2363H</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ω<sub>2</sub>= 4.51408</td><td align="left" valign="top" rowspan="1" colspan="1">2390T 2 <bold>2444S</bold> 2457L 2498L 2499F 2<bold>500F 2502K</bold> 2503N</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2514S 2516C 2522Y 2535L 2570S 2587R 2660C 2662M</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1"><bold>2666L</bold> 2667K 2668A <bold>2669M</bold> 2671T 2672S <bold>2673S</bold> 2677L</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1"><bold>2678G 2679L</bold> 2680Q <bold>2684K</bold> 2685P 2686F 2691H 2735W</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2743L 2748K 2756M 2818W 2821S 2822H 2823C 2827L</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2829G 2838A <bold>2839V</bold> 2964K 3012L <bold>3013R</bold> 3016S 3017N</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">3018S <bold>3019L</bold> 3023S <bold>3027P</bold> 3032P 3034P <bold>3036A</bold> 3037A</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">3040F <bold>3050F</bold> 3054L 3491P 3495V <bold>3774I 3775P</bold> 3777Q</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">3778R 3780Y 3793T 3808Y 3810Y 3816L 3830L 3832S</td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">M7</td><td align="left" valign="top" rowspan="2" colspan="1">Beta</td><td align="left" valign="top" rowspan="2" colspan="1">2</td><td align="left" valign="top" rowspan="2" colspan="1">−64609.64</td><td align="left" valign="top" rowspan="2" colspan="1">1.56036</td><td align="left" valign="top" rowspan="1" colspan="1">P = 0.45889</td><td align="left" valign="top" rowspan="1" colspan="1">Not allowed</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">q = 0.08925</td><td align="left" valign="top" rowspan="1" colspan="1"></td></tr><tr><td align="left" valign="top" rowspan="15" colspan="1">M8</td><td align="left" valign="top" rowspan="15" colspan="1">Beta and ω</td><td align="left" valign="top" rowspan="15" colspan="1">4</td><td align="left" valign="top" rowspan="15" colspan="1">−64284.21</td><td align="left" valign="top" rowspan="15" colspan="1">1.71973</td><td align="left" valign="top" rowspan="1" colspan="1">P<sub>0</sub>= 0.84072</td><td align="left" valign="top" rowspan="1" colspan="1">1Q 5N <bold>9L</bold> 15D 51E 181M 632K 670R 685G 883R 886G</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">P = 0.27207</td><td align="left" valign="top" rowspan="1" colspan="1">929S 1031W 1037A 1264T 1353E 1384R 1388S 1394H</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">q = 0.03464</td><td align="left" valign="top" rowspan="1" colspan="1">1400A 1413D 1418L 1737E 1738R 1742C 1760V 1769S</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">(P<sub>1</sub>= 0.15928)</td><td align="left" valign="top" rowspan="1" colspan="1">1770R 1787V <bold>1973R 1976R</bold> 1984R 1992A 1995S 2266L</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">ω = 4.34756</td><td align="left" valign="top" rowspan="1" colspan="1">2272N 2280L 2283S 2285S <bold>2298V 2304P</bold> 2305F <bold>2308N</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2352R 2362R 2363H 2390T 2 <bold>2444S</bold> 2457L 2498L 2499F</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2<bold>500F 2502K</bold> 2503N 2514S 2516C 2522Y 2535L <bold>2570S</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2587R 2660C 2662M <bold>2666L</bold> 2667K 2668A <bold>2669M</bold> 2671T</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2672S <bold>2673S</bold> 2677L <bold>2678G 2679L</bold> 2680Q <bold>2684K</bold> 2685P</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2686F 2691H 2735W 2743L 2748K 2756M 2817T 2818W</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2819M 2821S 2822H <bold>2823C</bold> 2827L 2829G 2838A <bold>2839V</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">2964K 3012L <bold>3013R</bold> 3016S 3017N 3018S <bold>3019L</bold> 3023S</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1"><bold>3027P</bold> 3032P 3034P <bold>3036A</bold> 3037A 3040F <bold>3050F</bold> 3054L</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">3491P 3495V <bold>3774I 3775P</bold> 3777Q 3778R 3780Y 3793T</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">3808Y 3810Y <bold>3816L</bold> 3830L 3832S</td></tr></tbody></table><table-wrap-foot><fn id="tfn3-ebo-9-2013-215"><p><bold>Notes:</bold> P represents the number of free parameters in the ω-distribution. Sites inferred to be under positive selection at the 99% level are bold and those at the 95% level are in italic.</p></fn></table-wrap-foot></table-wrap><table-wrap id="t4-ebo-9-2013-215" position="float"><label>Table 4</label><caption><p>Likelihood ratio statistics.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" valign="middle" rowspan="1" colspan="1"><bold>Comparison</bold></th><th align="left" valign="middle" rowspan="1" colspan="1"><bold>2Δℓ</bold></th><th align="left" valign="middle" rowspan="1" colspan="1"><bold>df</bold></th><th align="left" valign="middle" rowspan="1" colspan="1"><bold>P</bold></th><th align="left" valign="middle" rowspan="1" colspan="1"><bold>χ<sup>2</sup>1%</bold></th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">M1 (neutral) vs. M2 (selection)</td><td align="left" valign="top" rowspan="1" colspan="1">635.54</td><td align="left" valign="top" rowspan="1" colspan="1">2</td><td align="left" valign="top" rowspan="1" colspan="1">0.000E + 000</td><td align="left" valign="top" rowspan="1" colspan="1">9.21</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">M7 (beta) vs. M8 (beta and v)</td><td align="left" valign="top" rowspan="1" colspan="1">650.86</td><td align="left" valign="top" rowspan="1" colspan="1">2</td><td align="left" valign="top" rowspan="1" colspan="1">0.000E + 000</td><td align="left" valign="top" rowspan="1" colspan="1">9.21</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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