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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Comparative Transcriptome and iTRAQ Proteome Analyses of Citrus Root Responses to <italic>Candidatus</italic> Liberibacter asiaticus Infection</title><author><name sortKey="Zhong, Yun" sort="Zhong, Yun" uniqKey="Zhong Y" first="Yun" last="Zhong">Yun Zhong</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Cheng, Chun Zhen" sort="Cheng, Chun Zhen" uniqKey="Cheng C" first="Chun-Zhen" last="Cheng">Chun-Zhen Cheng</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jiang, Nong Hui" sort="Jiang, Nong Hui" uniqKey="Jiang N" first="Nong-Hui" last="Jiang">Nong-Hui Jiang</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jiang, Bo" sort="Jiang, Bo" uniqKey="Jiang B" first="Bo" last="Jiang">Bo Jiang</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zhang, Yong Yan" sort="Zhang, Yong Yan" uniqKey="Zhang Y" first="Yong-Yan" last="Zhang">Yong-Yan Zhang</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wu, Bo" sort="Wu, Bo" uniqKey="Wu B" first="Bo" last="Wu">Bo Wu</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Hu, Min Lun" sort="Hu, Min Lun" uniqKey="Hu M" first="Min-Lun" last="Hu">Min-Lun Hu</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zeng, Ji Wu" sort="Zeng, Ji Wu" uniqKey="Zeng J" first="Ji-Wu" last="Zeng">Ji-Wu Zeng</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Yan, Hua Xue" sort="Yan, Hua Xue" uniqKey="Yan H" first="Hua-Xue" last="Yan">Hua-Xue Yan</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Yi, Gan Jun" sort="Yi, Gan Jun" uniqKey="Yi G" first="Gan-Jun" last="Yi">Gan-Jun Yi</name><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zhong, Guang Yan" sort="Zhong, Guang Yan" uniqKey="Zhong G" first="Guang-Yan" last="Zhong">Guang-Yan Zhong</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26046530</idno><idno type="pmc">4457719</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4457719</idno><idno type="RBID">PMC:4457719</idno><idno type="doi">10.1371/journal.pone.0126973</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000150</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Comparative Transcriptome and iTRAQ Proteome Analyses of Citrus Root Responses to <italic>Candidatus</italic> Liberibacter asiaticus Infection</title><author><name sortKey="Zhong, Yun" sort="Zhong, Yun" uniqKey="Zhong Y" first="Yun" last="Zhong">Yun Zhong</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Cheng, Chun Zhen" sort="Cheng, Chun Zhen" uniqKey="Cheng C" first="Chun-Zhen" last="Cheng">Chun-Zhen Cheng</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jiang, Nong Hui" sort="Jiang, Nong Hui" uniqKey="Jiang N" first="Nong-Hui" last="Jiang">Nong-Hui Jiang</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jiang, Bo" sort="Jiang, Bo" uniqKey="Jiang B" first="Bo" last="Jiang">Bo Jiang</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zhang, Yong Yan" sort="Zhang, Yong Yan" uniqKey="Zhang Y" first="Yong-Yan" last="Zhang">Yong-Yan Zhang</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wu, Bo" sort="Wu, Bo" uniqKey="Wu B" first="Bo" last="Wu">Bo Wu</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Hu, Min Lun" sort="Hu, Min Lun" uniqKey="Hu M" first="Min-Lun" last="Hu">Min-Lun Hu</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zeng, Ji Wu" sort="Zeng, Ji Wu" uniqKey="Zeng J" first="Ji-Wu" last="Zeng">Ji-Wu Zeng</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Yan, Hua Xue" sort="Yan, Hua Xue" uniqKey="Yan H" first="Hua-Xue" last="Yan">Hua-Xue Yan</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Yi, Gan Jun" sort="Yi, Gan Jun" uniqKey="Yi G" first="Gan-Jun" last="Yi">Gan-Jun Yi</name><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zhong, Guang Yan" sort="Zhong, Guang Yan" uniqKey="Zhong G" first="Guang-Yan" last="Zhong">Guang-Yan Zhong</name><affiliation><nlm:aff id="aff001"><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff002"><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff003"><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Root samples of ‘Sanhu’ red tangerine trees infected with and without <italic>Candidatus</italic> Liberibacter asiaticus (<italic>C</italic>Las) were collected at 50 days post inoculation and subjected to RNA-sequencing and isobaric tags for relative and absolute quantification (iTRAQ) to profile the differentially expressed genes (DEGs) and proteins (DEPs), respectively. Quantitative real-time PCR was subsequently used to confirm the expression of 16 selected DEGs. Results showed that a total of 3956 genes and 78 proteins were differentially regulated by HLB-infection. Among the most highly up-regulated DEPs were sperm specific protein 411, copper ion binding protein, germin-like proteins, subtilisin-like proteins and serine carboxypeptidase-like 40 proteins whose transcript levels were concomitantly up-regulated as shown by RNA-seq data. Comparison between our results and those of the previously reported showed that known HLB-modulated biological pathways including cell-wall modification, protease-involved protein degradation, carbohydrate metabolism, hormone synthesis and signaling, transcription activities, and stress responses were similarly regulated by HLB infection but different or root-specific changes did exist. The root unique changes included the down-regulation in genes of ubiquitin-dependent protein degradation pathway, secondary metabolism, cytochrome P450s, UDP-glucosyl transferases and pentatricopeptide repeat containing proteins. Notably, nutrient absorption was impaired by HLB-infection as the expression of the genes involved in Fe, Zn, N and P adsorption and transportation were significantly changed. HLB-infection induced some cellular defense responses but simultaneously reduced the biosynthesis of the three major classes of secondary metabolites, many of which are known to have anti-pathogen activities. Genes involved in callose deposition were up-regulated whereas those involved in callose degradation were also up-regulated, indicating that the sieve tube elements in roots were hanging on the balance of life and death at this stage. In addition, signs of carbohydrate starvation were already eminent in roots at this stage. Other interesting genes and pathways that were changed by HLB-infection were also discussed based on our findings.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Batool, A" uniqKey="Batool A">A Batool</name></author><author><name sortKey="Iftikhar, Y" uniqKey="Iftikhar Y">Y Iftikhar</name></author><author><name sortKey="Mughal, Sm" uniqKey="Mughal S">SM Mughal</name></author><author><name sortKey="Khan, Mm" uniqKey="Khan M">MM Khan</name></author><author><name sortKey="Jaskani, Mj" uniqKey="Jaskani M">MJ Jaskani</name></author><author><name sortKey="Abbas, M" uniqKey="Abbas M">M Abbas</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Roman, Mp" uniqKey="Roman M">MP Román</name></author><author><name sortKey="Cambra, M" uniqKey="Cambra M">M Cambra</name></author><author><name sortKey="Juarez, J" uniqKey="Juarez J">J Juárez</name></author><author><name sortKey="Moreno, P" uniqKey="Moreno P">P 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26046530</article-id><article-id pub-id-type="pmc">4457719</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0126973</article-id><article-id pub-id-type="publisher-id">PONE-D-15-03499</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Comparative Transcriptome and iTRAQ Proteome Analyses of Citrus Root Responses to <italic>Candidatus</italic> Liberibacter asiaticus Infection</article-title><alt-title alt-title-type="running-head">Citrus Root Responses to CLas</alt-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Zhong</surname><given-names>Yun</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Cheng</surname><given-names>Chun-zhen</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jiang</surname><given-names>Nong-hui</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jiang</surname><given-names>Bo</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Yong-yan</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wu</surname><given-names>Bo</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hu</surname><given-names>Min-lun</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zeng</surname><given-names>Ji-wu</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yan</surname><given-names>Hua-xue</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yi</surname><given-names>Gan-jun</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhong</surname><given-names>Guang-yan</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref rid="cor001" ref-type="corresp">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R.China</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou, 510640, P.R.China</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Key Laboratory of Tropical and Subtropical Fruit Tree Researches, Guangdong Province, Guangzhou, 510640, P.R.China</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Liu</surname><given-names>Ji-Hong</given-names></name><role>Academic Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Key Laboratory of Horticultural Plant Biology (MOE), CHINA</addr-line></aff><author-notes><fn fn-type="conflict" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: YZ G-YZ C-ZC G-JY. Performed the experiments: YZ C-ZC Y-YZ N-HJ M-LH. Analyzed the data: C-ZC YZ BW. Contributed reagents/materials/analysis tools: N-HJ J-WZ BJ H-XY G-YZ. Wrote the paper: G-YZ YZ C-ZC.</p></fn><corresp id="cor001">* E-mail: <email>gy_zhong@163.com</email></corresp></author-notes><pub-date pub-type="epub"><day>5</day><month>6</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>10</volume><issue>6</issue><elocation-id>e0126973</elocation-id><history><date date-type="received"><day>24</day><month>1</month><year>2015</year></date><date date-type="accepted"><day>9</day><month>4</month><year>2015</year></date></history><permissions><copyright-year>2015</copyright-year><copyright-holder>Zhong et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p></license></permissions><self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0126973.pdf"></self-uri><abstract><p>Root samples of ‘Sanhu’ red tangerine trees infected with and without <italic>Candidatus</italic> Liberibacter asiaticus (<italic>C</italic>Las) were collected at 50 days post inoculation and subjected to RNA-sequencing and isobaric tags for relative and absolute quantification (iTRAQ) to profile the differentially expressed genes (DEGs) and proteins (DEPs), respectively. Quantitative real-time PCR was subsequently used to confirm the expression of 16 selected DEGs. Results showed that a total of 3956 genes and 78 proteins were differentially regulated by HLB-infection. Among the most highly up-regulated DEPs were sperm specific protein 411, copper ion binding protein, germin-like proteins, subtilisin-like proteins and serine carboxypeptidase-like 40 proteins whose transcript levels were concomitantly up-regulated as shown by RNA-seq data. Comparison between our results and those of the previously reported showed that known HLB-modulated biological pathways including cell-wall modification, protease-involved protein degradation, carbohydrate metabolism, hormone synthesis and signaling, transcription activities, and stress responses were similarly regulated by HLB infection but different or root-specific changes did exist. The root unique changes included the down-regulation in genes of ubiquitin-dependent protein degradation pathway, secondary metabolism, cytochrome P450s, UDP-glucosyl transferases and pentatricopeptide repeat containing proteins. Notably, nutrient absorption was impaired by HLB-infection as the expression of the genes involved in Fe, Zn, N and P adsorption and transportation were significantly changed. HLB-infection induced some cellular defense responses but simultaneously reduced the biosynthesis of the three major classes of secondary metabolites, many of which are known to have anti-pathogen activities. Genes involved in callose deposition were up-regulated whereas those involved in callose degradation were also up-regulated, indicating that the sieve tube elements in roots were hanging on the balance of life and death at this stage. In addition, signs of carbohydrate starvation were already eminent in roots at this stage. Other interesting genes and pathways that were changed by HLB-infection were also discussed based on our findings.</p></abstract><funding-group><funding-statement>This work was supported by the International Science & Technology Cooperation Program of China (2012DFA30610, G-YZ received the funding), by the Guangdong provincial Science and technology Programs (S2013010015149, YZ received the funding; 2012B050700006, YZ received the funding; 2013B090700007, G-YZ received the funding).</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="4"></table-count><page-count count="21"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front><body><sec sec-type="intro" id="sec001"><title>Introduction</title><p>Citrus Huanglongbing (HLB), the most destructive and still uncontrollable disease, has been responsible for the loss of tens of millions of trees worldwide and generated tremendous economic losses to the citrus industries [<xref rid="pone.0126973.ref001" ref-type="bibr">1</xref>–<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>]. The causative agents, <italic>Candidatus</italic> Liberibacters, are gram-negative, phloem-inhabiting <italic>α-Proteobacteria</italic>. Currently three species, i.e., the heat-tolerant <italic>Ca</italic>. Liberibacter asiaticus (<italic>C</italic>Las), the heat-sensitive <italic>Ca</italic>. L. africanus (<italic>C</italic>Laf) and the recently identified heat tolerant <italic>Ca</italic>. L. americanus (<italic>C</italic>Lam), have been identified on <italic>Citrus</italic> [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>, <xref rid="pone.0126973.ref004" ref-type="bibr">4</xref>]. It is known that <italic>C</italic>Las is the most pathogenic of the three species. <italic>C</italic>Las can be transmitted by grafting with HLB-infected budwoods and by phloem-feeding psyllid, <italic>Diaphorina citri</italic>. Traditionally, HLB management practices include use of disease free nursery trees, control of citrus psyllid, and eradication of infected trees [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>, <xref rid="pone.0126973.ref005" ref-type="bibr">5</xref>], but the effectiveness of these measures varies with the levels of social and technical development. Efforts in breeding for HLB-resistance have not yielded satisfactory results for lack of resistance genes in <italic>Citrus</italic> [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>]. Pyramiding resistance genes may offer a possible solution to HLB as shown by breeding for disease resistance in rice, wheat and barley [<xref rid="pone.0126973.ref006" ref-type="bibr">6</xref>–<xref rid="pone.0126973.ref008" ref-type="bibr">8</xref>]. But this strategy requires a through understanding of the host-pathogen interactions especially the QTLs involved.</p><p>Following colonization in citrus trees, the HLB pathogen disperses quickly and will spread to all tissues and organs including roots within three months to one year. Typical symptoms on diseased trees include variegated chlorosis of leaves, abnormal coloration of fruit, and dieback of twigs, among others, and eventually collapse of the trees in 2 to 5 years [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>]. Fruit quality is adversely affected and often sourer and bitter [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. Seed germination and seedling growth are also affected [<xref rid="pone.0126973.ref010" ref-type="bibr">10</xref>]. Biochemically, infected trees accumulate unusual high levels of starches in photosynthetic cells, phloem elements and vascular parenchyma cells of leaves and petioles, and in cells of xylem parenchyma and phelloderm of stems [<xref rid="pone.0126973.ref011" ref-type="bibr">11</xref>, <xref rid="pone.0126973.ref012" ref-type="bibr">12</xref>]. The accumulation of starches is assumed to be resulted from phloem plugging associated with not only the bacteria growing inside but also callose deposition and accumulation of phloem proteins [<xref rid="pone.0126973.ref013" ref-type="bibr">13</xref>]. Chlorosis of leaves and shoots was reported to have a link with deficiency in minerals of N, Fe, Mg, and Zn [<xref rid="pone.0126973.ref014" ref-type="bibr">14</xref>, <xref rid="pone.0126973.ref015" ref-type="bibr">15</xref>], and with disruption of chloroplast inner grana structure caused by excessively accumulated starches [<xref rid="pone.0126973.ref013" ref-type="bibr">13</xref>]. Transcriptomic studies showed that photosynthesis and carbohydrate metabolism genes, among many others, are abnormally expressed in leaves [<xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>–<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>], stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>] and fruits [<xref rid="pone.0126973.ref023" ref-type="bibr">23</xref>, <xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>]. In general, starch metabolism genes are down-regulated in all examined tissues, and photosynthesis genes are down-regulated in leaves and stems but not in fruits [<xref rid="pone.0126973.ref023" ref-type="bibr">23</xref>, <xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>]. MicroRNA (miRNA) profiles were reportedly changed in leaves and the findings that the phosphorus-starvation induced miR399 was significantly induced and that the P level was significantly reduced had inspired the authors to apply phosphorus to remit the diseased trees, which was reportedly to have significantly alleviated HLB symptoms [<xref rid="pone.0126973.ref025" ref-type="bibr">25</xref>].</p><p>It has long been assumed that the roots of HLB-infected trees should have suffered from starvation of carbohydrates [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>, <xref rid="pone.0126973.ref026" ref-type="bibr">26</xref>]. This is because the phloem cells constituting the carbohydrate passage from leaves to roots will be gradually blocked directly or indirectly by the continuously multiplying bacteria, resulting in an increasing reduction in the supply of carbohydrates to roots. Apparently, carbohydrate starvation will reduce the growth and activity of the roots, which will, in turn, cause a reduction in absorption and supply of minerals to the above ground tissues, thus further aggravating chlorosis symptoms. Indeed, starch depletion was observed in diseased roots by microscopy studies [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. A more than 30% of reduction in fibrous root mass was observed in <italic>C</italic>Las infected sweet orange (<italic>Citrus sinensis</italic>) [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]. Changes in expression of 111 genes were also found in <italic>C</italic>Las infected roots [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. Even though, evidence accumulated so far is not sufficient to elucidate the role of roots in the development of HLB symptoms and the molecular events induced by HLB-infection.</p><p>Global changes in expression of genes have provided valuable clues to the elucidation of the pathogenesis of plant diseases including bacterial diseases [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>]. Modern genetics studies have shown that most genes exercise their roles through their protein products. Intuitively, a gene’s high level of transcripts should represent a correspondingly high level of its proteins. However, it has been extensively documented that posttranscriptional regulations, including translation, post-translational modification and degradation of the proteins determine to a large extent the actual levels of almost all proteins [<xref rid="pone.0126973.ref028" ref-type="bibr">28</xref>]. Therefore, to obtain a more correct picture about the role of a gene, its protein level should also be measured. In this study, we used respectively the RNA-seq and an eight-channel iTRAQ (isobaric tags for relative and absolute quantification) technique to analyze the genome-wide gene expression changes and to identify differentially expressed proteins in roots of ‘Sanhu’ red tangerine (<italic>C</italic>. <italic>reticulata</italic> Blanco cv. ‘Sanhu’) infected with <italic>C</italic>Las bacteria. ‘Sanhu’ red tangerine is a traditional rootstock and widely used in south China for the production of two important mandarins, ‘Shatangju’ (<italic>C</italic>. <italic>reticulata</italic> Blanco cv. ‘Shatangju’) and ‘Gonggan’ (<italic>C</italic>. <italic>reticulata</italic> Blanco cv. ‘Gonggan’). However, trees on ‘Sanhu’ red tangerine are very susceptible to <italic>C</italic>Las. Our aim is to identify the early <italic>C</italic>Las-responsive genes in roots with the hope that some of them may be exploited in breeding for HLB resistance and in developing a method to mitigating HLB symptoms of the diseased trees in the future.</p></sec><sec sec-type="results" id="sec002"><title>Results</title><sec id="sec003"><title>Comparative transcriptome analysis of <italic>C</italic>Las-affected and control ‘Sanhu’ red tangerine roots by Illumina sequencing</title><p>Two-year-old ‘Sanhu’ red tangerine seedlings were treated by graft-inoculation of <italic>C</italic>Las-carrying buds and healthy buds respectively. The inoculated trees were detected by PCR for the presence of <italic>C</italic>Las bacteria in leaves and roots once every 10 days. It was shown that no inoculated trees became HLB positive in both leaves and roots until 50 dpi (days post inoculation). These early HLB positive trees were then sampled together with the control trees for roots, from which total RNA and total protein were extracted.</p><p>RNA-seq generated approximately 52.9 million and 49.6 million 90-bp pair-end reads respectively for HLB-free control (C) and HLB-infected (H) root RNA samples. About 79.72% of C and 78.53% of H total reads were successfully mapped to <italic>C</italic>. <italic>clementina</italic> genome, and 63.06% and 60.72% of them matched with their corresponding transcripts in the archived gene sequence databases.</p><p>A ∣log<sub>2</sub>[fold change]∣ of ≥ 1 (p-value <0.005, FDR ≤0.001) was used to identify differentially expressed genes (DEGs). As a result, a total of 3956 DEGs were identified, 1840 of them were up-regulated and the rest 2116 were down-regulated (<xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref>). Kyoto encyclopedia of genes and genomes (KEGG) analysis showed that 19 pathways were significantly enriched (p-value <0.05 and q-value <0.05) (<xref rid="pone.0126973.t001" ref-type="table">Table 1</xref>). Notably, DEGs involved in ‘plant-pathogen interaction pathway’ accounted for about 19% of the DEGs assigned to different pathways (<xref rid="pone.0126973.t001" ref-type="table">Table 1</xref>).</p><table-wrap id="pone.0126973.t001" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.t001</object-id><label>Table 1</label><caption><title>The 19 significantly enriched pathways identified by Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis (p-value <0.05; q-value <0.05).</title></caption><alternatives><graphic id="pone.0126973.t001g" xlink:href="pone.0126973.t001"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="left" rowspan="1" colspan="1">Rank</th><th align="left" rowspan="1" colspan="1">Pathway</th><th align="left" rowspan="1" colspan="1">DEGs with pathway annotation (2312)</th><th align="left" rowspan="1" colspan="1">All genes with pathway annotation (14097)</th><th align="left" rowspan="1" colspan="1">p-value</th><th align="left" rowspan="1" colspan="1">q-value</th><th align="left" rowspan="1" colspan="1">Pathway ID</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1">Stilbenoid, diarylheptanoid and gingerol biosynthesis</td><td align="left" rowspan="1" colspan="1">114 (4.93%)</td><td align="left" rowspan="1" colspan="1">360 (2.55%)</td><td align="left" rowspan="1" colspan="1">3.21E-13</td><td align="left" rowspan="1" colspan="1">3.85E-11</td><td align="left" rowspan="1" colspan="1">ko00945</td></tr><tr><td align="left" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1">Phenylpropanoid biosynthesis</td><td align="left" rowspan="1" colspan="1">134 (5.8%)</td><td align="left" rowspan="1" colspan="1">476 (3.38%)</td><td align="left" rowspan="1" colspan="1">3.92E-11</td><td align="left" rowspan="1" colspan="1">2.35E-09</td><td align="left" rowspan="1" colspan="1">ko00940</td></tr><tr><td align="left" rowspan="1" colspan="1">3</td><td align="left" rowspan="1" colspan="1">Plant-pathogen interaction</td><td align="left" rowspan="1" colspan="1">434 (18.77%)</td><td align="left" rowspan="1" colspan="1">2052 (14.56%)</td><td align="left" rowspan="1" colspan="1">5.92E-10</td><td align="left" rowspan="1" colspan="1">2.37E-08</td><td align="left" rowspan="1" colspan="1">ko04626</td></tr><tr><td align="left" rowspan="1" colspan="1">4</td><td align="left" rowspan="1" colspan="1">Limonene and pinene degradation</td><td align="left" rowspan="1" colspan="1">76 (3.29%)</td><td align="left" rowspan="1" colspan="1">253 (1.79%)</td><td align="left" rowspan="1" colspan="1">3.73E-08</td><td align="left" rowspan="1" colspan="1">1.12E-06</td><td align="left" rowspan="1" colspan="1">ko00903</td></tr><tr><td align="left" rowspan="1" colspan="1">5</td><td align="left" rowspan="1" colspan="1">Plant hormone signal transduction</td><td align="left" rowspan="1" colspan="1">255 (11.03%)</td><td align="left" rowspan="1" colspan="1">1170 (8.3%)</td><td align="left" rowspan="1" colspan="1">3.01E-07</td><td align="left" rowspan="1" colspan="1">7.21E-06</td><td align="left" rowspan="1" colspan="1">ko04075</td></tr><tr><td align="left" rowspan="1" colspan="1">6</td><td align="left" rowspan="1" colspan="1">Biosynthesis of secondary metabolites</td><td align="left" rowspan="1" colspan="1">394 (17.04%)</td><td align="left" rowspan="1" colspan="1">1966 (13.95%)</td><td align="left" rowspan="1" colspan="1">2.48E-06</td><td align="left" rowspan="1" colspan="1">4.96E-05</td><td align="left" rowspan="1" colspan="1">ko01110</td></tr><tr><td align="left" rowspan="1" colspan="1">7</td><td align="left" rowspan="1" colspan="1">Glucosinolate biosynthesis</td><td align="left" rowspan="1" colspan="1">25 (1.08%)</td><td align="left" rowspan="1" colspan="1">65 (0.46%)</td><td align="left" rowspan="1" colspan="1">1.59E-05</td><td align="left" rowspan="1" colspan="1">0.000273</td><td align="left" rowspan="1" colspan="1">ko00966</td></tr><tr><td align="left" rowspan="1" colspan="1">8</td><td align="left" rowspan="1" colspan="1">Flavonoid biosynthesis</td><td align="left" rowspan="1" colspan="1">98 (4.24%)</td><td align="left" rowspan="1" colspan="1">413 (2.93%)</td><td align="left" rowspan="1" colspan="1">6.26E-05</td><td align="left" rowspan="1" colspan="1">0.000938</td><td align="left" rowspan="1" colspan="1">ko00941</td></tr><tr><td align="left" rowspan="1" colspan="1">9</td><td align="left" rowspan="1" colspan="1">Tryptophan metabolism</td><td align="left" rowspan="1" colspan="1">33 (1.43%)</td><td align="left" rowspan="1" colspan="1">110 (0.78%)</td><td align="left" rowspan="1" colspan="1">0.000263</td><td align="left" rowspan="1" colspan="1">0.003487</td><td align="left" rowspan="1" colspan="1">ko00380</td></tr><tr><td align="left" rowspan="1" colspan="1">10</td><td align="left" rowspan="1" colspan="1">ABC transporters</td><td align="left" rowspan="1" colspan="1">34 (1.47%)</td><td align="left" rowspan="1" colspan="1">115 (0.82%)</td><td align="left" rowspan="1" colspan="1">0.000291</td><td align="left" rowspan="1" colspan="1">0.003487</td><td align="left" rowspan="1" colspan="1">ko02010</td></tr><tr><td align="left" rowspan="1" colspan="1">11</td><td align="left" rowspan="1" colspan="1">Phenylalanine metabolism</td><td align="left" rowspan="1" colspan="1">46 (1.99%)</td><td align="left" rowspan="1" colspan="1">171 (1.21%)</td><td align="left" rowspan="1" colspan="1">0.000322</td><td align="left" rowspan="1" colspan="1">0.003515</td><td align="left" rowspan="1" colspan="1">ko00360</td></tr><tr><td align="left" rowspan="1" colspan="1">12</td><td align="left" rowspan="1" colspan="1">alpha-Linolenic acid metabolism</td><td align="left" rowspan="1" colspan="1">37 (1.6%)</td><td align="left" rowspan="1" colspan="1">141 (1%)</td><td align="left" rowspan="1" colspan="1">0.001911</td><td align="left" rowspan="1" colspan="1">0.019111</td><td align="left" rowspan="1" colspan="1">ko00592</td></tr><tr><td align="left" rowspan="1" colspan="1">13</td><td align="left" rowspan="1" colspan="1">Zeatin biosynthesis</td><td align="left" rowspan="1" colspan="1">36 (1.56%)</td><td align="left" rowspan="1" colspan="1">138 (0.98%)</td><td align="left" rowspan="1" colspan="1">0.002433</td><td align="left" rowspan="1" colspan="1">0.02246</td><td align="left" rowspan="1" colspan="1">ko00908</td></tr><tr><td align="left" rowspan="1" colspan="1">14</td><td align="left" rowspan="1" colspan="1">Flavone and flavonol biosynthesis</td><td align="left" rowspan="1" colspan="1">48 (2.08%)</td><td align="left" rowspan="1" colspan="1">211 (1.5%)</td><td align="left" rowspan="1" colspan="1">0.009841</td><td align="left" rowspan="1" colspan="1">0.084352</td><td align="left" rowspan="1" colspan="1">ko00944</td></tr><tr><td align="left" rowspan="1" colspan="1">15</td><td align="left" rowspan="1" colspan="1">Metabolic pathways</td><td align="left" rowspan="1" colspan="1">540 (23.36%)</td><td align="left" rowspan="1" colspan="1">3066 (21.75%)</td><td align="left" rowspan="1" colspan="1">0.022176</td><td align="left" rowspan="1" colspan="1">0.177407</td><td align="left" rowspan="1" colspan="1">ko01100</td></tr><tr><td align="left" rowspan="1" colspan="1">16</td><td align="left" rowspan="1" colspan="1">Biosynthesis of unsaturated fatty acids</td><td align="left" rowspan="1" colspan="1">18 (0.78%)</td><td align="left" rowspan="1" colspan="1">70 (0.5%)</td><td align="left" rowspan="1" colspan="1">0.030787</td><td align="left" rowspan="1" colspan="1">0.230902</td><td align="left" rowspan="1" colspan="1">ko01040</td></tr><tr><td align="left" rowspan="1" colspan="1">17</td><td align="left" rowspan="1" colspan="1">Pentose and glucuronate interconversions</td><td align="left" rowspan="1" colspan="1">38 (1.64%)</td><td align="left" rowspan="1" colspan="1">173 (1.23%)</td><td align="left" rowspan="1" colspan="1">0.03315</td><td align="left" rowspan="1" colspan="1">0.233999</td><td align="left" rowspan="1" colspan="1">ko00040</td></tr><tr><td align="left" rowspan="1" colspan="1">18</td><td align="left" rowspan="1" colspan="1">Alanine, aspartate and glutamate metabolism</td><td align="left" rowspan="1" colspan="1">19 (0.82%)</td><td align="left" rowspan="1" colspan="1">77 (0.55%)</td><td align="left" rowspan="1" colspan="1">0.040075</td><td align="left" rowspan="1" colspan="1">0.267169</td><td align="left" rowspan="1" colspan="1">ko00250</td></tr><tr><td align="left" rowspan="1" colspan="1">19</td><td align="left" rowspan="1" colspan="1">Starch and sucrose metabolism</td><td align="left" rowspan="1" colspan="1">68 (2.94%)</td><td align="left" rowspan="1" colspan="1">341 (2.42%)</td><td align="left" rowspan="1" colspan="1">0.045885</td><td align="left" rowspan="1" colspan="1">0.289797</td><td align="left" rowspan="1" colspan="1">ko00500</td></tr></tbody></table></alternatives></table-wrap></sec><sec id="sec004"><title>iTRAQ-based comparative proteomic analysis of <italic>C</italic>Las-affected and healthy ‘Sanhu’ red tangerine roots</title><p>A total of 1455 proteins were identified from <italic>C</italic>Las infected and control root samples. A one by one search found that 1233 (92.78%) of the 1455 identified proteins had corresponding transcripts in our RNA-seq data. In the end, 78 proteins were identified as differentially expressed proteins (DEPs) at p-value <0.05 and a cutoff value of >|±1.5|-fold, which included 46 up-regulated and 32 down-regulated proteins (<xref rid="pone.0126973.t002" ref-type="table">Table 2</xref> and <xref rid="pone.0126973.s003" ref-type="supplementary-material">S2 Table</xref>). An expression correlation analysis was performed between these proteins and their corresponding transcripts, and a Pearson correlation coefficient of ~0.41 was obtained, indicating a moderate positive correlation existed between transcriptomic and proteomic data (<xref rid="pone.0126973.s001" ref-type="supplementary-material">S1 Fig</xref>).</p><table-wrap id="pone.0126973.t002" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.t002</object-id><label>Table 2</label><caption><title>Differentially expressed proteins identified in <italic>C</italic>Las-infected ‘Sanhu’ red tangerine roots.</title></caption><alternatives><graphic id="pone.0126973.t002g" xlink:href="pone.0126973.t002"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="left" rowspan="1" colspan="1">Gene ID<xref rid="t002fn001" ref-type="table-fn">*</xref></th><th align="left" rowspan="1" colspan="1">Gene description</th><th align="left" rowspan="1" colspan="1">Protein Fold change</th><th align="left" rowspan="1" colspan="1">Gene Fold change</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">clementine0.9_003979m/Ciclev10018836m</td><td align="left" rowspan="1" colspan="1">Sperm specific protein 411 (SSP411)</td><td align="char" char="." rowspan="1" colspan="1">6.475</td><td align="char" char="." rowspan="1" colspan="1">-1.523</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_029368m/Ciclev10024168m</td><td align="left" rowspan="1" colspan="1">Copper ion binding protein</td><td align="char" char="." rowspan="1" colspan="1">4.783</td><td align="char" char="." rowspan="1" colspan="1">5.856</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_028487m/Ciclev10030149m</td><td align="left" rowspan="1" colspan="1">Germin-like protein</td><td align="char" char="." rowspan="1" colspan="1">4.137</td><td align="char" char="." rowspan="1" colspan="1">4.720</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_035803m/Ciclev10023551m</td><td align="left" rowspan="1" colspan="1">Subtilisin-like protease</td><td align="char" char="." rowspan="1" colspan="1">3.976</td><td align="char" char="." rowspan="1" colspan="1">4.047</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_002904m/Ciclev10027863m</td><td align="left" rowspan="1" colspan="1">Subtilisin-like protease-like</td><td align="char" char="." rowspan="1" colspan="1">3.926</td><td align="char" char="." rowspan="1" colspan="1">5.530</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_033258m/Ciclev10018003m</td><td align="left" rowspan="1" colspan="1">Germin-like protein</td><td align="char" char="." rowspan="1" colspan="1">3.284</td><td align="char" char="." rowspan="1" colspan="1">3.410</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_030770m/Ciclev10018062m</td><td align="left" rowspan="1" colspan="1">SCPL40 (serine carboxypeptidase-like 40)</td><td align="char" char="." rowspan="1" colspan="1">3.138</td><td align="char" char="." rowspan="1" colspan="1">8.143</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_028660m/Ciclev10007081m</td><td align="left" rowspan="1" colspan="1">Major allergen mal d1</td><td align="char" char="." rowspan="1" colspan="1">2.989</td><td align="char" char="." rowspan="1" colspan="1">1.762</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_021650m/Ciclev10022211m</td><td align="left" rowspan="1" colspan="1">Trypsin and protease inhibitor family protein</td><td align="char" char="." rowspan="1" colspan="1">2.964</td><td align="char" char="." rowspan="1" colspan="1">-1.190</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_003047m/Ciclev10000364m</td><td align="left" rowspan="1" colspan="1">Subtilisin-like protease</td><td align="char" char="." rowspan="1" colspan="1">2.721</td><td align="char" char="." rowspan="1" colspan="1">0.772</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_021318m/Ciclev10029251m</td><td align="left" rowspan="1" colspan="1">GLP5 (germin-like protein 5)</td><td align="char" char="." rowspan="1" colspan="1">2.169</td><td align="char" char="." rowspan="1" colspan="1">0.552</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_023327m/Ciclev10026538m</td><td align="left" rowspan="1" colspan="1">Lipid-associated family protein</td><td align="char" char="." rowspan="1" colspan="1">2.139</td><td align="char" char="." rowspan="1" colspan="1">-0.266</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_026109m/Ciclev10029627m</td><td align="left" rowspan="1" colspan="1">40s ribosomal protein s25-2</td><td align="char" char="." rowspan="1" colspan="1">2.095</td><td align="char" char="." rowspan="1" colspan="1">1.206</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_027200m/Ciclev10013189m</td><td align="left" rowspan="1" colspan="1">Ubiquinol-cytochrome c reductase complex 8.0 kDa protein</td><td align="char" char="." rowspan="1" colspan="1">2.014</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_017579m/Ciclev10028975m</td><td align="left" rowspan="1" colspan="1">Plasma membrane intrinsic protein 2;4</td><td align="char" char="." rowspan="1" colspan="1">1.96</td><td align="char" char="." rowspan="1" colspan="1">-1.694</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_017092m/Ciclev10021381m</td><td align="left" rowspan="1" colspan="1">Pre-mRNA-splicing factor SF2</td><td align="char" char="." rowspan="1" colspan="1">1.918</td><td align="char" char="." rowspan="1" colspan="1">-0.912</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_017463m/Ciclev10028959m</td><td align="left" rowspan="1" colspan="1">PR3 (basic chitinase)</td><td align="char" char="." rowspan="1" colspan="1">1.905</td><td align="char" char="." rowspan="1" colspan="1">-1.199</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_024393m/Ciclev10022655m</td><td align="left" rowspan="1" colspan="1">Major pollen allergen Car b 1 isoforms 1A and 1B</td><td align="char" char="." rowspan="1" colspan="1">1.881</td><td align="char" char="." rowspan="1" colspan="1">0.265</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_015410m/Ciclev10026050m</td><td align="left" rowspan="1" colspan="1">Peroxidase</td><td align="char" char="." rowspan="1" colspan="1">1.859</td><td align="char" char="." rowspan="1" colspan="1">0.592</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_025955m/Ciclev10006259m</td><td align="left" rowspan="1" colspan="1">60s ribosomal protein L30</td><td align="char" char="." rowspan="1" colspan="1">1.83</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_024868m/Ciclev10029528m</td><td align="left" rowspan="1" colspan="1">PR4 (Pathogenesis-related 4)</td><td align="char" char="." rowspan="1" colspan="1">1.788</td><td align="char" char="." rowspan="1" colspan="1">1.230</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_001766m/Ciclev10030651m</td><td align="left" rowspan="1" colspan="1">ATP binding protein</td><td align="char" char="." rowspan="1" colspan="1">1.768</td><td align="char" char="." rowspan="1" colspan="1">-0.641</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_014340m/Ciclev10008748m</td><td align="left" rowspan="1" colspan="1">Cysteine-type peptidase</td><td align="char" char="." rowspan="1" colspan="1">1.746</td><td align="char" char="." rowspan="1" colspan="1">0.670</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_024894m/Ciclev10029532m</td><td align="left" rowspan="1" colspan="1">40S ribosomal protein S23</td><td align="char" char="." rowspan="1" colspan="1">1.739</td><td align="char" char="." rowspan="1" colspan="1">0.611</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_011012m/Ciclev10004931m</td><td align="left" rowspan="1" colspan="1">PKT3 (Peroxisomal 3-ketoacyl-CoA thiolase 3)</td><td align="char" char="." rowspan="1" colspan="1">1.733</td><td align="char" char="." rowspan="1" colspan="1">-0.449</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_021972m/Ciclev10006241m</td><td align="left" rowspan="1" colspan="1">23.5 kDa mitochondrial small heat shock protein</td><td align="char" char="." rowspan="1" colspan="1">1.706</td><td align="char" char="." rowspan="1" colspan="1">1.063</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_022028m/Ciclev10005897m</td><td align="left" rowspan="1" colspan="1">Embryo-specific protein</td><td align="char" char="." rowspan="1" colspan="1">1.702</td><td align="char" char="." rowspan="1" colspan="1">-0.777</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_002926m/Ciclev10000352m</td><td align="left" rowspan="1" colspan="1">Glycosyl hydrolase family 3 protein</td><td align="char" char="." rowspan="1" colspan="1">1.687</td><td align="char" char="." rowspan="1" colspan="1">0.595</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_008158m/Ciclev10028242m</td><td align="left" rowspan="1" colspan="1">Leucine-rich repeat family protein</td><td align="char" char="." rowspan="1" colspan="1">1.673</td><td align="char" char="." rowspan="1" colspan="1">0.380</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_020929m</td><td align="left" rowspan="1" colspan="1">Peptidase m</td><td align="left" rowspan="1" colspan="1"></td><td align="char" char="." rowspan="1" colspan="1">0.173</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_007997m/Ciclev10011525m</td><td align="left" rowspan="1" colspan="1">Aspartic proteinase</td><td align="char" char="." rowspan="1" colspan="1">1.665</td><td align="char" char="." rowspan="1" colspan="1">0.022</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_015076m</td><td align="left" rowspan="1" colspan="1">Peroxidase 27</td><td align="left" rowspan="1" colspan="1"></td><td align="char" char="." rowspan="1" colspan="1">0.715</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_005969m/Ciclev10025245m</td><td align="left" rowspan="1" colspan="1">LPR1 (Low Phosphate Root1)</td><td align="char" char="." rowspan="1" colspan="1">1.613</td><td align="char" char="." rowspan="1" colspan="1">-0.932</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_012976m/Ciclev10008649m</td><td align="left" rowspan="1" colspan="1">Plastocyanin-like domain-containing protein</td><td align="char" char="." rowspan="1" colspan="1">1.606</td><td align="char" char="." rowspan="1" colspan="1">-0.018</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_002976m/Ciclev10014355m</td><td align="left" rowspan="1" colspan="1">Subtilisin-like protease</td><td align="char" char="." rowspan="1" colspan="1">1.603</td><td align="char" char="." rowspan="1" colspan="1">0.329</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_025727m/Ciclev10022906m</td><td align="left" rowspan="1" colspan="1">Inhibitor of trypsin and hageman factor</td><td align="char" char="." rowspan="1" colspan="1">1.595</td><td align="char" char="." rowspan="1" colspan="1">-2.133</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_019843m/Ciclev10021884m</td><td align="left" rowspan="1" colspan="1">Expansin-like b1-like</td><td align="char" char="." rowspan="1" colspan="1">1.583</td><td align="char" char="." rowspan="1" colspan="1">-0.556</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_024747m/Ciclev10029263m</td><td align="left" rowspan="1" colspan="1">Histone H2B</td><td align="char" char="." rowspan="1" colspan="1">1.578</td><td align="char" char="." rowspan="1" colspan="1">0.068</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_020531m/Ciclev10002349m</td><td align="left" rowspan="1" colspan="1">Dehydrin 1</td><td align="char" char="." rowspan="1" colspan="1">1.565</td><td align="char" char="." rowspan="1" colspan="1">0.123</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_008435m/Ciclev10015027m</td><td align="left" rowspan="1" colspan="1">Glycosyl hydrolase family 17 protein</td><td align="char" char="." rowspan="1" colspan="1">1.544</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_024798m/Ciclev10017092m</td><td align="left" rowspan="1" colspan="1">Eukaryotic translation initiation factor 1A</td><td align="char" char="." rowspan="1" colspan="1">1.543</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_026229m/Ciclev10017280m</td><td align="left" rowspan="1" colspan="1">NADH-ubiquinone oxidoreductase b18 subunit</td><td align="char" char="." rowspan="1" colspan="1">1.525</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_020331m/Ciclev10032615m</td><td align="left" rowspan="1" colspan="1">Auxin-induced in root cultures protein 12</td><td align="char" char="." rowspan="1" colspan="1">1.524</td><td align="char" char="." rowspan="1" colspan="1">1.011</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_003766m/Ciclev10030843m</td><td align="left" rowspan="1" colspan="1">unknown protein</td><td align="char" char="." rowspan="1" colspan="1">1.506</td><td align="char" char="." rowspan="1" colspan="1">0.254</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_008447m/Ciclev10015024m</td><td align="left" rowspan="1" colspan="1">SCPL40 (serine carboxypeptidase-like 40)</td><td align="char" char="." rowspan="1" colspan="1">1.503</td><td align="char" char="." rowspan="1" colspan="1">1.505</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_025240m/Ciclev10006199m</td><td align="left" rowspan="1" colspan="1">60s ribosomal protein L22-2</td><td align="char" char="." rowspan="1" colspan="1">1.502</td><td align="char" char="." rowspan="1" colspan="1">0.336</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_011579m/Ciclev10008467m</td><td align="left" rowspan="1" colspan="1">Eukaryotic translation initiation factor 4A1</td><td align="char" char="." rowspan="1" colspan="1">-1.504</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_022971m/Ciclev10026349m</td><td align="left" rowspan="1" colspan="1">Nicotinamidase</td><td align="char" char="." rowspan="1" colspan="1">-1.508</td><td align="char" char="." rowspan="1" colspan="1">-1.150</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_023835m/Ciclev10032923m</td><td align="left" rowspan="1" colspan="1">ATP synthase d chain</td><td align="char" char="." rowspan="1" colspan="1">-1.511</td><td align="char" char="." rowspan="1" colspan="1">0.941</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_001010m/Ciclev10007294m</td><td align="left" rowspan="1" colspan="1">Disease resistance protein (NBS-LRR class)</td><td align="char" char="." rowspan="1" colspan="1">-1.515</td><td align="char" char="." rowspan="1" colspan="1">-0.823</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_011647m/Ciclev10001330m</td><td align="left" rowspan="1" colspan="1">DNAJ heat shock N-terminal domain-containing protein</td><td align="char" char="." rowspan="1" colspan="1">-1.517</td><td align="char" char="." rowspan="1" colspan="1">0.629</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_001400m/Ciclev10018691m</td><td align="left" rowspan="1" colspan="1">Cell division cycle 5-like protein</td><td align="char" char="." rowspan="1" colspan="1">-1.520</td><td align="char" char="." rowspan="1" colspan="1">-0.375</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_013575m/Ciclev10028695m</td><td align="left" rowspan="1" colspan="1">Pantothenate kinase</td><td align="char" char="." rowspan="1" colspan="1">-1.527</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_018717m/Ciclev10027333m</td><td align="left" rowspan="1" colspan="1">Calcium ion binding</td><td align="char" char="." rowspan="1" colspan="1">-1.546</td><td align="char" char="." rowspan="1" colspan="1">-0.299</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_021984m/Ciclev10016269m</td><td align="left" rowspan="1" colspan="1">Syntaxin 23</td><td align="char" char="." rowspan="1" colspan="1">-1.546</td><td align="char" char="." rowspan="1" colspan="1">-0.001</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_023333m/Ciclev10006024m</td><td align="left" rowspan="1" colspan="1">40s ribosomal protein s10-like</td><td align="char" char="." rowspan="1" colspan="1">-1.567</td><td align="char" char="." rowspan="1" colspan="1">0.336</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_034011m</td><td align="left" rowspan="1" colspan="1">Benzoate carboxyl</td><td align="char" char="." rowspan="1" colspan="1">-1.582</td><td align="char" char="." rowspan="1" colspan="1">0.979</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_029071m/Ciclev10006465m</td><td align="left" rowspan="1" colspan="1">FAD-binding domain-containing protein</td><td align="char" char="." rowspan="1" colspan="1">-1.592</td><td align="char" char="." rowspan="1" colspan="1">0.430</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_012453m/Ciclev10025804m</td><td align="left" rowspan="1" colspan="1">Chalcone synthase 2</td><td align="char" char="." rowspan="1" colspan="1">-1.603</td><td align="char" char="." rowspan="1" colspan="1">1.088</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_026642m/Ciclev10002973m</td><td align="left" rowspan="1" colspan="1">Acyl-CoA-binding protein 6</td><td align="char" char="." rowspan="1" colspan="1">-1.613</td><td align="char" char="." rowspan="1" colspan="1">0.642</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_025382m/Ciclev10017167m</td><td align="left" rowspan="1" colspan="1">Programmed cell death protein 5</td><td align="char" char="." rowspan="1" colspan="1">-1.629</td><td align="char" char="." rowspan="1" colspan="1">0.359</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_025950m/Ciclev10013051m</td><td align="left" rowspan="1" colspan="1">60s acidic ribosomal protein P2</td><td align="char" char="." rowspan="1" colspan="1">-1.645</td><td align="char" char="." rowspan="1" colspan="1">0.420</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_001048m</td><td align="left" rowspan="1" colspan="1">Unknown protein</td><td align="char" char="." rowspan="1" colspan="1">-1.669</td><td align="char" char="." rowspan="1" colspan="1">-0.892</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_021243m/Ciclev10005840m</td><td align="left" rowspan="1" colspan="1">Glutathione transferase</td><td align="char" char="." rowspan="1" colspan="1">-1.672</td><td align="char" char="." rowspan="1" colspan="1">-1.421</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_007327m/Ciclev10024917m</td><td align="left" rowspan="1" colspan="1">Phospholipase D alpha 1</td><td align="char" char="." rowspan="1" colspan="1">-1.686</td><td align="char" char="." rowspan="1" colspan="1">-0.096</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_002685m/Ciclev10019696m</td><td align="left" rowspan="1" colspan="1">Glutamate-cysteine ligase</td><td align="char" char="." rowspan="1" colspan="1">-1.686</td><td align="char" char="." rowspan="1" colspan="1">-0.129</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_016514m/Ciclev10001924m</td><td align="left" rowspan="1" colspan="1">Meprin and TRAF homology domain-containing protein</td><td align="char" char="." rowspan="1" colspan="1">-1.689</td><td align="char" char="." rowspan="1" colspan="1">1.524</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_003119m/Ciclev10014376m</td><td align="left" rowspan="1" colspan="1">Calcium-binding EF hand family protein</td><td align="char" char="." rowspan="1" colspan="1">-1.724</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_018424m/Ciclev10016241m</td><td align="left" rowspan="1" colspan="1">Proteasome subunit beta type</td><td align="char" char="." rowspan="1" colspan="1">-1.751</td><td align="char" char="." rowspan="1" colspan="1">0.191</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_017608m/Ciclev10032291m</td><td align="left" rowspan="1" colspan="1">Alpha-soluble NSF attachment protein</td><td align="char" char="." rowspan="1" colspan="1">-1.779</td><td align="char" char="." rowspan="1" colspan="1">0.186</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_028964m</td><td align="left" rowspan="1" colspan="1">Beta-caryophyllene synthase</td><td align="char" char="." rowspan="1" colspan="1">-1.880</td><td align="char" char="." rowspan="1" colspan="1">-0.796</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_025957m/Ciclev10033122m</td><td align="left" rowspan="1" colspan="1">Tubulin-specific chaperone A</td><td align="char" char="." rowspan="1" colspan="1">-1.890</td><td align="char" char="." rowspan="1" colspan="1">0.057</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_026048m/Ciclev10013168m</td><td align="left" rowspan="1" colspan="1">Vacuolar ATP synthase subunit G 1</td><td align="char" char="." rowspan="1" colspan="1">-1.908</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_014859m/Ciclev10008832m</td><td align="left" rowspan="1" colspan="1">Farnesyl pyrophosphate synthetase</td><td align="char" char="." rowspan="1" colspan="1">-1.916</td><td align="left" rowspan="1" colspan="1">-</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_014472m/Ciclev10028483m</td><td align="left" rowspan="1" colspan="1">Vacuolar sorting protein 4b</td><td align="char" char="." rowspan="1" colspan="1">-1.923</td><td align="char" char="." rowspan="1" colspan="1">0.745</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_007126m/Ciclev10000432m</td><td align="left" rowspan="1" colspan="1">Unknown protein</td><td align="char" char="." rowspan="1" colspan="1">-2.045</td><td align="char" char="." rowspan="1" colspan="1">-0.348</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_024367m/Ciclev10016953m</td><td align="left" rowspan="1" colspan="1">-</td><td align="char" char="." rowspan="1" colspan="1">-2.288</td><td align="char" char="." rowspan="1" colspan="1">-0.230</td></tr><tr><td align="left" rowspan="1" colspan="1">clementine0.9_020940m/Ciclev10029230m</td><td align="left" rowspan="1" colspan="1">Metal ion binding protein</td><td align="char" char="." rowspan="1" colspan="1">-2.421</td><td align="char" char="." rowspan="1" colspan="1">0.775</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t002fn001"><p>*: ‘/’ separates the IDs of the same gene (old version (Cclementina_165)/new version (Cclementina_182));-: not available</p></fn></table-wrap-foot></table-wrap><p>Of the DEPs, a sperm specific protein 411 (SSP411) (Ciclev10018836m) was noteworthy for the protein was up-regulated by more than 6-fold while its mRNA level was slightly decreased by about 1.5-fold in HLB-infected roots. The copper ion binding protein (Ciclev10024168m) was increased by 4.78-fold, and a concomitant increase of 5.86-fold was also found for its transcripts. A germin-like protein (Ciclev10030149m) showed a 4.1-fold and a 4.78-fold increases in its protein and mRNA levels, respectively. Another germin-like protein (Ciclev10018003m) was similarly up-regulated (increased by 3.3-fold in protein level and 3.4-fold in mRNA level). A SCPL40 (serine carboxypeptidase-like 40) protein was up-regulated by > 3-fold and > 8-fold respectively in protein and mRNA levels. Two of the 4 subtilisin-like protease DEPs were found to be also up-regulated in their mRNA level but the other two were not. We identified also 3 up-regulated DEPs (leucine-rich repeat family protein, glycosyl hydrolase family 3 protein, expansin-like B1) in roots (<xref rid="pone.0126973.g001" ref-type="fig">Fig 1</xref> and <xref rid="pone.0126973.s003" ref-type="supplementary-material">S2 Table</xref>). Interestingly, more than 10% of the DEPs were associated with protein degradation (<xref rid="pone.0126973.t002" ref-type="table">Table 2</xref> and <xref rid="pone.0126973.s003" ref-type="supplementary-material">S2 Table</xref>).</p><fig id="pone.0126973.g001" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.g001</object-id><label>Fig 1</label><caption><title>Mapman analysis for differentailly expressed genes (A) and diferentially expressed proteins (B) involved in metabolic pathways.</title><p>Red squares represent genes or proteins that were significantly up-regulated; green squares represent genes or proteins that were significantly down-regulated.</p></caption><graphic xlink:href="pone.0126973.g001"></graphic></fig></sec><sec id="sec005"><title>Gene pathway enrichment analysis of <italic>C</italic>Las-modulated host pathways</title><p>PageMan analysis showed that no significantly enriched pathways were associated with the DEPs identified in this study. However, this was not the case when the same analysis was applied to DEGs since not only down-regulated pathways but also up-regulated pathways were identified (<xref rid="pone.0126973.t003" ref-type="table">Table 3</xref>). The up-regulated pathways were cell wall modification, cysteine and aspartate protease mediated protein degradation, sugar and nutrient physiology signaling, receptor kinases signaling, and calcium signaling while the down-regulated pathways were regulation of transcription and ubiquitin-dependent protein degradation. In addition, 3 down-regulated protein gene families, <italic>cytochrome P450</italic>, <italic>UDP glucosyl and glucoronyl transferases</italic> (<italic>UGTs</italic>) and <italic>pentatricopeptide repeat containing proteins</italic> (<italic>PPRRPs</italic>), and one up-regulated <italic>β-1</italic>, <italic>3-glucan hydrolase</italic> gene family (<italic>βGlu</italic>) were classified into the ‘not assigned’ by PageMan.</p><table-wrap id="pone.0126973.t003" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.t003</object-id><label>Table 3</label><caption><title>PageMan display of <italic>C</italic>Las-modulated pathways identified by RNA-seq.</title></caption><alternatives><graphic id="pone.0126973.t003g" xlink:href="pone.0126973.t003"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="left" rowspan="1" colspan="1">Bin</th><th align="left" rowspan="1" colspan="1">Bin description</th><th align="left" rowspan="1" colspan="1">p-value</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><bold>30</bold></td><td align="left" rowspan="1" colspan="1"><bold>Signaling</bold></td><td align="left" rowspan="1" colspan="1"><bold>2.83E-05</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>10.7</bold></td><td align="left" rowspan="1" colspan="1"><bold>Cell wall. modification</bold></td><td align="left" rowspan="1" colspan="1"><bold>1.06E-04</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">35.1.5</td><td align="left" rowspan="1" colspan="1">Not assigned. no ontology. PPRRP</td><td align="left" rowspan="1" colspan="1">1.40E-04</td></tr><tr><td align="left" rowspan="1" colspan="1">29.5.11</td><td align="left" rowspan="1" colspan="1">Protein. degradation. ubiquitin</td><td align="left" rowspan="1" colspan="1">1.51E-04</td></tr><tr><td align="left" rowspan="1" colspan="1">29.5.11.4</td><td align="left" rowspan="1" colspan="1">Protein. degradation. ubiquitin.E3</td><td align="left" rowspan="1" colspan="1">3.88E-04</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>30.3</bold></td><td align="left" rowspan="1" colspan="1"><bold>Signaling. calcium</bold></td><td align="left" rowspan="1" colspan="1"><bold>3.88E-04</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">26.1</td><td align="left" rowspan="1" colspan="1">Misc. cytochrome P450</td><td align="left" rowspan="1" colspan="1">5.27E-04</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>30.2</bold></td><td align="left" rowspan="1" colspan="1"><bold>Signaling. receptor kinases</bold></td><td align="left" rowspan="1" colspan="1"><bold>6.99E-04</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>30.2.17</bold></td><td align="left" rowspan="1" colspan="1"><bold>Signaling. receptor kinases. DUF 26</bold></td><td align="left" rowspan="1" colspan="1"><bold>0.001199</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">27.3</td><td align="left" rowspan="1" colspan="1">RNA. regulation of transcription</td><td align="left" rowspan="1" colspan="1">0.00317</td></tr><tr><td align="left" rowspan="1" colspan="1">29.5.11.4.3.2</td><td align="left" rowspan="1" colspan="1">Protein. degradation. ubiquitin. E3. SCF. FBOX</td><td align="left" rowspan="1" colspan="1">0.003335</td></tr><tr><td align="left" rowspan="1" colspan="1">29.5.11.4.3</td><td align="left" rowspan="1" colspan="1">Protein. degradation. ubiquitin. E3. SCF</td><td align="left" rowspan="1" colspan="1">0.00392</td></tr><tr><td align="left" rowspan="1" colspan="1">27</td><td align="left" rowspan="1" colspan="1">RNA</td><td align="left" rowspan="1" colspan="1">0.004422</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>29.5.3</bold></td><td align="left" rowspan="1" colspan="1"><bold>Protein. degradation. cysteine protease</bold></td><td align="left" rowspan="1" colspan="1"><bold>0.009876</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>29.5.4</bold></td><td align="left" rowspan="1" colspan="1"><bold>Protein. degradation. aspartate protease</bold></td><td align="left" rowspan="1" colspan="1"><bold>0.009876</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>30.1</bold></td><td align="left" rowspan="1" colspan="1"><bold>Signaling. in sugar and nutrient physiology</bold></td><td align="left" rowspan="1" colspan="1"><bold>0.009935</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">35.1</td><td align="left" rowspan="1" colspan="1">Not assigned. no ontology</td><td align="left" rowspan="1" colspan="1">0.019032</td></tr><tr><td align="left" rowspan="1" colspan="1">27.3.8</td><td align="left" rowspan="1" colspan="1">RNA. regulation of transcription. C2C2(Zn) DOF zinc finger family</td><td align="left" rowspan="1" colspan="1">0.034666</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>26.4</bold></td><td align="left" rowspan="1" colspan="1"><bold>Misc. beta-1,3-glucan hydrolases</bold></td><td align="left" rowspan="1" colspan="1"><bold>0.038032</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">26.2</td><td align="left" rowspan="1" colspan="1">Misc. UDP glucosyl and glucoronyl transferases</td><td align="left" rowspan="1" colspan="1">0.049359</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t003fn001"><p>Note: Up-regulated pathways are highlighted in bold; PPRRP: pentatricopeptide repeat containing protein; DUF: domain of unknown function; SCF: F-box containing complex; DOF: DNA binding with one finger.</p></fn></table-wrap-foot></table-wrap><p>Analysis showed the largest proportion of the DEGs were related to biotic and abiotic stress responses since 434 and 1164 DEGs were categorized into the ‘plant and pathogen interaction’ and the ‘stress-related’ when analyzed by KEGG (<xref rid="pone.0126973.t001" ref-type="table">Table 1</xref>) and by MapMan (<xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref> and <xref rid="pone.0126973.g002" ref-type="fig">Fig 2</xref>), respectively. Representative DEGs were 2 <italic>RIN4</italic> (<italic>RPM1 interacting protein 4</italic>), 7 <italic>MEKK1</italic>, 5 <italic>JAZ</italic> (<italic>Jasmonate-ZIM-domain protein</italic>), 1 <italic>HSP90</italic> (<italic>heat shock protein 90</italic>), 3 <italic>PR1</italic> (<italic>pathogenesis-related 1</italic>), 1 <italic>NPR1</italic>, 1 <italic>ALD1</italic> (<italic>AGD2-like defense response protein 1</italic>), and 12 of the 13 <italic>βGlu</italic> that were the up-regulated. Notably, one of the <italic>βGlu</italic> genes, <italic>BG1</italic>, was even up-regulated by more than 10-fold. Some PR proteins such as PR3 and PR4 were also shown to be up-regulated.</p><fig id="pone.0126973.g002" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.g002</object-id><label>Fig 2</label><caption><title>Mapman analysis for differentailly expressed genes (A) and diferentially expressed proteins (B) involved in stress response.</title><p>Red squares represent genes or proteins that were significantly up-regulated; green squares represent genes or proteins that were significantly down-regulated.</p></caption><graphic xlink:href="pone.0126973.g002"></graphic></fig><p>Around 400 DEGs that were assigned to the category of ‘regulation of transcription’. Among them were 44 <italic>AP2/EREBPs</italic>, 42 <italic>MYBs</italic>, 30 <italic>C2H2 zinc finger family proteins</italic> and 28 <italic>bHLHs</italic>, which were either up- or down-regulated even if they were from the same family. However, DEGs from some families including 6 <italic>ARF</italic> and 6 <italic>TCP</italic> family members were all down-regulated, and those from the <italic>C2H2 zinc finger family</italic>, the <italic>homeobox transcription factor family</italic>, the <italic>GRAS transcription factor family</italic>, and the <italic>bZIP transcription factor family</italic> were mostly down-regulated. Contrastingly, DEGs from some other families including 1 <italic>PUB23</italic> and 1 <italic>PUB24</italic> of the <italic>PHOR1</italic> family were only up-regulated, and those from the <italic>WRKY</italic> domain transcription factor family were mostly up-regulated. In addition, many DEGs of this category were unclassifiable, including 2 <italic>CDR1</italic> (<italic>constitutive disease resistance 1</italic>) that were up-regulated by 5.2- and 4.6-fold respectively, and 1 <italic>aspartyl protease family protein</italic> (ciclev10020250m) that was up-regulated by 5.8-fold.</p><p>A large proportion of DEGs, totaled at 308, were related to cell signaling, including 113 <italic>leucine rich repeat XI protein</italic> (LRR) genes and 67 <italic>DUF 26</italic> (<italic>domain of unknown function</italic>) <italic>receptor kinase</italic> genes, and 39 calcium signaling genes. The up- and the down-regulated DEGs of LRR were more or less equal in number, but calcium signaling related DEGs and <italic>DUF26s</italic> were mostly up-regulated.</p><p>Two hundred and twenty four DEGs were assigned to the category of ‘protein degradation’ including 135 ubiquitin-related genes, 17 subtilase-related genes, 12 cysteine protease-related genes, 14 aspartate protease-related genes, 9 serine-protease-related genes and 16 AAA type ATPase-related genes. The ubiquitin-related DEGs were mostly down-regulated, but the protease-related DEGs were mostly up-regulated.</p></sec><sec id="sec006"><title>Comparison between DEGs in roots and those in other tissues</title><p>A comparison was made between our results and those of leaves [<xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>–<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>], fruits [<xref rid="pone.0126973.ref023" ref-type="bibr">23</xref>, <xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>] and stems and roots [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>], and the results were summarized in <xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>. As shown in the table, DEGs from different tissues that have been analyzed so far were mostly involved in sugar and starch metabolism, cell wall metabolism, stress responses, hormone signaling, signaling and transcription factors, transport, cell organization and development, and protein metabolism.</p><table-wrap id="pone.0126973.t004" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.t004</object-id><label>Table 4</label><caption><title>Comparison of <italic>C</italic>Las-regulated pathways in citrus leaves, fruits, stems and roots.</title></caption><alternatives><graphic id="pone.0126973.t004g" xlink:href="pone.0126973.t004"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col><col align="left" valign="middle" span="1"></col></colgroup><thead><tr><th align="left" rowspan="1" colspan="1">Pathways</th><th align="left" rowspan="1" colspan="1">Leaves</th><th align="left" rowspan="1" colspan="1">Fruits</th><th align="left" rowspan="1" colspan="1">Stems</th><th align="left" rowspan="1" colspan="1">Roots</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><bold>Sugar and starch metabolism</bold></td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>AGPase</italic>, <italic>AAM</italic>, <italic>SS</italic>, <italic>GBSS</italic> [<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>]; <bold>Down</bold>: <italic>BAM</italic>, <italic>SPS</italic> [<xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>], <italic>SUS</italic> [<xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>];</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>Invertase</italic>, galactinol metabolism, <bold>DR</bold>: starch metabolism and raffinose synthesis [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>APL3</italic>, <italic>GBSS</italic>, <italic>AMY</italic>, <italic>myo-inositol oxygenase</italic>; <bold>Down</bold>: <italic>BAM1</italic>, <italic>neutral invertase</italic>, trehalose biosynthesis [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>SS</italic>, <italic>AGPases</italic>, <italic>fructokinase</italic>, <italic>invertases</italic>, <italic>hexokinases</italic>, trehalose biosynthesis and myo-inositol metabolism; <bold>Down</bold>: <italic>PGSIP4</italic>, <italic>SUS3</italic>, <italic>HGL1</italic>, <italic>BAM3</italic>, <italic>BAM6</italic></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Cell wall metabolism</bold></td><td align="left" rowspan="1" colspan="1">Mostly up-regulated [<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>] or down-regulated [<xref rid="pone.0126973.ref023" ref-type="bibr">23</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly up-regulated [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly down-regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: cell wall modification and pectin esterases related</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Stress responses</bold></td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>, <xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly up-regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Hormone signaling</bold></td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: ethylene, SA and JA related; <bold>Down</bold>: cytokinins and gibberellins related [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: SA and JA related; <bold>Down</bold>: ABA related [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Down</bold>: cytokinin, ABA and GA related; <bold>DR</bold>: JA, auxin and ethylene related</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Signaling and transcription factors</bold></td><td align="left" rowspan="1" colspan="1">Differentially regulated; <bold>Up</bold>: <italic>MYB</italic>s, <italic>WRKYs</italic>, <italic>LRRs</italic>; <bold>Down</bold>: <italic>AP2</italic> [<xref rid="pone.0126973.ref017" ref-type="bibr">17</xref>, <xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated; <bold>Up</bold>: <italic>leucine-rich repeat (LRR) receptor kinases</italic>, <italic>DUF26</italic> and <italic>WRKY</italic>s [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated; <bold>Up</bold>: <italic>receptor like kniases</italic>; <bold>Down</bold>: calcium signaling [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: MYB [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>], <italic>DUF26</italic>, <italic>WRKYs</italic>, calcium signaling and sugar and nutrient physiology signaling related; <bold>Down</bold>: light signaling; <bold>DR</bold>: <italic>LRRs</italic></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Transport</bold></td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>zinc transporters</italic>; <bold>Down</bold>: major intrinsic proteins [<xref rid="pone.0126973.ref017" ref-type="bibr">17</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially-regulated; <bold>Up</bold>: Sugar, sulfur, ABC transporter and ammonium related transporters [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>metal</italic>, <italic>peptide</italic>, <italic>oligopeptides</italic>, <italic>ions phosphate and nitrate transporter</italic>; <bold>Down</bold>: major intrinsic proteins [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: <italic>Zinc</italic>, <italic>copper</italic>, <italic>some phosphate and metabolite transporters</italic>; <bold>Down</bold>: <italic>nitrate transporters</italic>, major intrinsic proteins, sugar, sulfur, amino acids, nucleotide, metal, peptide and oligopeptides transport related</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Protein metabolism</bold></td><td align="left" rowspan="1" colspan="1">Down-regulated [<xref rid="pone.0126973.ref017" ref-type="bibr">17</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: Protein degradation and misfolding;<bold>Down</bold>: Protein synthesis [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: Protein synthesis, protease mediated protein degradation, <bold>Down</bold>: protein degradation [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]; ubiquitin-dependent protein degradation</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Photosynthesis</bold></td><td align="left" rowspan="1" colspan="1">Down-regulated [<xref rid="pone.0126973.ref017" ref-type="bibr">17</xref>, <xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>, <xref rid="pone.0126973.ref025" ref-type="bibr">25</xref>]</td><td align="left" rowspan="1" colspan="1">Up-regulated [<xref rid="pone.0126973.ref026" ref-type="bibr">26</xref>, <xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly down-regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly down-regulated</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Secondary metabolism</bold></td><td align="left" rowspan="1" colspan="1">Mostly up-regulated [<xref rid="pone.0126973.ref025" ref-type="bibr">25</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]; <bold>Down</bold>: flavonoid biosynthesis [<xref rid="pone.0126973.ref026" ref-type="bibr">26</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly up-regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1"><bold>Up</bold>: alkaloid metabolism related; <bold>Down</bold>: Phenlypropanoids, isoprenoids and flavonoids metabolisms,</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Energy metabolism</bold></td><td align="left" rowspan="1" colspan="1">Up-regulated [<xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>, <xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>]</td><td align="left" rowspan="1" colspan="1">Up-regulated [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1">Up-regulated</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Cell organization</bold></td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>, <xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">Differentially regulated [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]</td><td align="left" rowspan="1" colspan="1">Mostly up-regulated</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Cell cycle and cell division</bold></td><td align="left" rowspan="1" colspan="1">Down-regulated [<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>]</td><td align="left" rowspan="1" colspan="1">Down-regulated [<xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]</td><td align="left" rowspan="1" colspan="1">-</td><td align="left" rowspan="1" colspan="1">Down-regulated</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Phloem proteins</bold></td><td align="left" rowspan="1" colspan="1"><bold>Up:</bold><italic>PP2-B15</italic> [<xref rid="pone.0126973.ref020" ref-type="bibr">20</xref>–<xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>, <xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>]; <italic>PP2-B10</italic>, <italic>PP2-B14</italic> [<xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>]</td><td align="left" rowspan="1" colspan="1">-</td><td align="left" rowspan="1" colspan="1">-</td><td align="left" rowspan="1" colspan="1"><bold>Up:</bold><italic>PP2-B10</italic>, <italic>2-B15</italic>, <italic>2-B11</italic>, <italic>PP2-A13</italic>, <italic>PP2-A1</italic> and <italic>PP2-A9</italic></td></tr></tbody></table></alternatives><table-wrap-foot><fn id="t004fn001"><p>Note: Up: up-regulated genes or pathways; Down: down-regulated genes or pathways; DR: pathways or genes differently regulated; the italic are genes;-: not available; AGPase: ADP-glucose pyrophosphorylase; AAM: alpha-amylase; BAM: Beta-amylase; SS: starch synthase; GBSS: granule bound starch synthase; SUS: sucrose synthase; SPS: sucrose-phosphate synthase; PGSIP4: plant glycogenin-like starch initiation protein; HGL1: heteroglycan glucosidase 1; APL3: ADP-glucose pyrophosphorylase large subunit 3; LRR: leucine-rich repeat; DUF: domain of unknown function; PP: phloem protein</p></fn></table-wrap-foot></table-wrap><p>The trends in expression of the DEGs identified in roots by this study were generally consistent with those identified in the above ground tissues. For example, most DEGs of sugar and starch metabolism related protein modification related proteins, WRKYs, and energy metabolism related proteins were commonly up-regulated, while those related to cell cycle and cell division down-regulated, in all tissues (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>, Figs <xref rid="pone.0126973.g001" ref-type="fig">1</xref> and <xref rid="pone.0126973.g002" ref-type="fig">2</xref>). The <italic>β-amylase</italic> (<italic>BAM</italic>) and <italic>sucrose synthase</italic> (<italic>SUS</italic>) genes down-regulated in the above tissues were also down-regulated in roots. <italic>Glucan synthase-Like 7</italic> (<italic>GSL7</italic>), a gene tightly coexpressed with two <italic>SUS</italic> genes [<xref rid="pone.0126973.ref029" ref-type="bibr">29</xref>], was down-regulated not only in <italic>C</italic>Lam-infected leaves but also in our <italic>C</italic>Las-infected roots. It was reported that several <italic>phloem protein 2</italic> (<italic>PP2</italic>) genes were up-regulated in HLB-infected leaves [<xref rid="pone.0126973.ref017" ref-type="bibr">17</xref>–<xref rid="pone.0126973.ref019" ref-type="bibr">19</xref>, <xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>], and in this study, 6 <italic>PP2</italic> DEGs were up-regulated with <italic>PP2-B10</italic> and <italic>PP2-B15</italic> as the most highly up-regulated as shown by a up-regulation of 10- and 12-fold respectively in their transcript levels in <italic>C</italic>Las-infected roots (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref> and <xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref>). Most protein degradation related DEGs that were up-regulated in many HLB infected tissues were also up-regulated in roots, including those of <italic>subtilases</italic>, <italic>cysteine proteases</italic>, <italic>aspartate proteases</italic>, <italic>serine proteases</italic>, and <italic>AAA-type ATPase family proteins</italic>, and comparatively, more DEGs of these categories were present in roots than in other tissues. DEGs involved in hormone metabolism and signaling pathways were also similarly modulated by <italic>C</italic>Las in different tissues (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>).</p><p>However, some DEGs were oppositely regulated in roots as compared with one or more above-ground tissues. Some cell wall metabolism-related DEGs such as <italic>pectin esterase</italic> genes were down-regulated in stem [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>] but most of them were up-regulated in leaves [<xref rid="pone.0126973.ref019" ref-type="bibr">19</xref>], fruits [<xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>] and roots (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>). Photosynthesis related genes down-regulated in leaves and stems were also down-regulated in non-photosynthetic roots as shown in this study (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>) but they were up-regulated in fruits [<xref rid="pone.0126973.ref023" ref-type="bibr">23</xref>, <xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>]. On the contrary, calcium signaling related DEGs were down-regulated in stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>] but most of them were up-regulated in roots (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>). Ubiquitin-dependent protein degradation related genes were either not regulated or up-regulated in the above ground tissues [<xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>] but most of them were down-regulated in roots (<xref rid="pone.0126973.g003" ref-type="fig">Fig 3</xref>). Similarly, most of the secondary metabolism related genes were up-regulated in the above ground tissues [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>, <xref rid="pone.0126973.ref022" ref-type="bibr">22</xref>], but they were mostly down-regulated in roots. Nearly 3/4 of the 104 <italic>cytochrome P450 monooxygenase</italic> DEGs were down-regulated in roots (<xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref>). But one of them, <italic>CYP83B1</italic>, whose protein is involved in biosynthesis of glucosinolates and callose deposition [<xref rid="pone.0126973.ref030" ref-type="bibr">30</xref>] was up-regulated in <italic>C</italic>Lam-infected leaves [<xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>]. Although some of the 7 <italic>CYP83B1</italic> DEGs were also up-regulated in HLB-infected roots, the remaining others were down-regulated. A total of 203 transport related DEGs were identified in roots (<xref rid="pone.0126973.g004" ref-type="fig">Fig 4</xref>), but comparatively there were only 39 of them in stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. Moreover, far more HLB-regulated ABC transporter DEGs were found in our study. Z<italic>inc transporter precursor</italic> (<italic>ZIP</italic>) genes were up-regulated in leaves [<xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>], and agreeably, 3 up-regulated <italic>ZIP</italic> genes were identified in roots. Five of the 10 phosphate transport-related DEGs including 2 <italic>PHT3</italic> (<italic>phosphate transporter 3</italic>), 1 <italic>PHT1;1</italic>, 1 <italic>PHT4;6</italic>, and 1 <italic>phosphate transmembrane transporter</italic> were up-regulated, and <italic>PHT3</italic> and the <italic>PHT1</italic> were even up-regulated by more than 7-fold but the rest 5 were down-regulated in roots; in comparison, only one of them, <italic>PHT3</italic>, was found to be up-regulated in stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. Two nitrate transporter genes, <italic>NRT2</italic>:<italic>1</italic> (<italic>nitrate transporter 2</italic>:<italic>1</italic>) and <italic>NRT2</italic>:<italic>5</italic>, were both down-regulated in roots whereas two different nitrate transporter genes, <italic>NRT1</italic> and <italic>NRT1</italic>:<italic>2</italic>, were up-regulated in stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. We identified also 2 highly up-regulated <italic>AMT2</italic> (<italic>ammonium transporter 2</italic>) genes (ciclev10023275m, 4.6-fold; ciclev10010379m, 12-fold) and one highly down-regulated <italic>AMT1</italic>:<italic>2</italic> (ciclev10019808m, -4-fold) while previous reports did not mention any of them as DEG.</p><fig id="pone.0126973.g003" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.g003</object-id><label>Fig 3</label><caption><title>Mapman analysis for differentailly expressed genes (A) and diferentially expressed proteins (B) involved in ubiquitin-dependent protein degradation.</title><p>Red squares represent genes or proteins that were significantly up-regulated; green squares represent genes or proteins that were significantly down-regulated.</p></caption><graphic xlink:href="pone.0126973.g003"></graphic></fig><fig id="pone.0126973.g004" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.g004</object-id><label>Fig 4</label><caption><title>Mapman analysis for differentailly expressed genes (A) and diferentially expressed proteins (B) involved in transportation.</title><p>Red squares represent genes or proteins that were significantly up-regulated; green squares represent genes or proteins that were significantly down-regulated.</p></caption><graphic xlink:href="pone.0126973.g004"></graphic></fig><p>Root specific changes were also observed for many DEGs. For example, many metal transporter genes were down-regulated while only a few or no such DEGs were identified in the above ground tissues. Three <italic>ferric reduction oxidase</italic> (<italic>FRO</italic>) genes, <italic>FRO2</italic>, <italic>FRO7</italic> and <italic>FRO8</italic>, were down-regulated in roots but not significantly changed in the above ground tissues of the HLB-infected trees. Another striking finding in our root results was that as many as 94 DEGs, 86 of which were down-regulated, were from the largest plant protein gene family <italic>PPRRP</italic> since no such DEGs were reported in previous studies involving the above ground tissues.</p></sec><sec id="sec007"><title>Changes in expression of DEGs in roots following <italic>C</italic>Las infection</title><p>Quantitative real-time PCR (qRT-PCR) was performed to investigate the changes in transcription of 16 typical HLB-modulated genes in roots at 20 dpi and 50 dpi. As shown in <xref rid="pone.0126973.g005" ref-type="fig">Fig 5</xref>, the expression of all the investigated genes in roots of 50 dpi was consistent between qRT-PCR and RNA-seq data, showing that the quality of our RNA-seq data was acceptable. Comparison of the data between the two time points revealed 4 expression patterns: 1) a almost constant up-regulation at both 20 dpi and 50 dpi, as represented by <italic>NPR1</italic>, <italic>invertase</italic> and <italic>ACR4</italic>; 2) a moderate increase at 20 dpi followed by a more significant increase at 50 dpi as represented by <italic>RIN4</italic>, <italic>RPS2</italic>, <italic>DPI</italic>, <italic>PP2-B15</italic>, <italic>TPP</italic>, <italic>XTR6</italic>, <italic>CRPK</italic>; 3) a moderate down-regulation at 20 dpi followed by a more significant down-regulation at 50 dpi as represented by <italic>BAM</italic>, <italic>KCS6</italic> and <italic>PMEI</italic>; and 4) a initial significant down-regulation at 20 dpi followed by a moderate down-regulation at 50 dpi as represented by <italic>BRI1</italic> and <italic>BZIP</italic>.</p><fig id="pone.0126973.g005" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0126973.g005</object-id><label>Fig 5</label><caption><title>Expression of 16 differentially expressed genes at 20 dpi (A) and 50 dpi (B) as determined by quantitative real time PCR.</title><p>C indicates the expression level determined by RNA-seq. <italic>RIN4</italic>: <italic>RPM1 interacting protein 4</italic>; <italic>RPS2</italic>: <italic>disease resistant protein ribosomal protein S2</italic>; <italic>NPR1</italic>: <italic>regulatory protein nonexpresser of PR genes 1</italic>; <italic>DRP</italic>: <italic>disease resistant protein (TIR-NBS-LRR class)</italic>; <italic>PP2-B15</italic>: <italic>Phloem protein 2-B15</italic>; <italic>BAM</italic>: <italic>β-amylase</italic>; <italic>PMEI</italic>: <italic>pectin methylesterase inhibitor</italic>; <italic>TPP</italic>: <italic>trehalose-6-phosphate phosphatase</italic>; <italic>XTR6</italic>: <italic>Xyloglucan endotransglycosylase 6</italic>; <italic>BZIP</italic>: <italic>bZIP transcription factor</italic>; <italic>CRPK</italic>: <italic>cysteine-rich protein kinase</italic>; <italic>ACR4</italic>: <italic>Act repeat 4</italic>; <italic>BRI1</italic>: <italic>BRI1 kinase inhibitor 1</italic>; <italic>KCS6</italic>: <italic>3-ketoacyl-CoA synthase 6</italic>.</p></caption><graphic xlink:href="pone.0126973.g005"></graphic></fig></sec></sec><sec sec-type="conclusions" id="sec008"><title>Discussion</title><p>HLB bacteria can be vectored from diseased trees to healthy trees by ACP (Asian citrus psyllids), a species of tiny insect that is difficult to control in open field [<xref rid="pone.0126973.ref031" ref-type="bibr">31</xref>]. Therefore, the hope of bringing the disease under control relies on developing new cultivars with HLB resistance [<xref rid="pone.0126973.ref026" ref-type="bibr">26</xref>]. However, facing with the problems of long juvenile period, large tree size, frequently occurred polyembryonic seeds, and no available resistance genes, breeding for HLB resistant citrus by hybridization has so far made little progress. Alternatively, transgenic citrus should intimately offer a solution to the problem [<xref rid="pone.0126973.ref032" ref-type="bibr">32</xref>]. But efficient transgenic engineering work requires knowing where the host innate defense system is breached by the invading bacteria. Studies have showed that changes in transcriptome and proteome in host following pathogen infection can provide important clues to the mechanism of pathogenesis and suggest candidate genes or pathways for engineering for resistance. In <italic>Citrus</italic>, transcriptomic studies have been conducted in leaves, stems and fruits of HLB-infected trees [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>, <xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>–<xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>], and proteomic study was also conducted in leaves [<xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>]. These studies have accumulated a large body of information about the molecular mechanism of HLB-host interactions. However, roots are largely neglected though evidence showed that roots are equally susceptible to and can be quickly colonized by HLB bacteria [<xref rid="pone.0126973.ref003" ref-type="bibr">3</xref>, <xref rid="pone.0126973.ref027" ref-type="bibr">27</xref>]. The only transcriptional analysis involving roots of HLB-infected Valencia orange showed that only 111 DEGs were detected by microarray [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. Given the importance of roots in absorption and transportation of nutrients and in offering mechanical support to the whole tree, roots may differ significantly in their responses to HLB-infection than other tissues.</p><p>In this study we used respectively RNA-seq and iTRAQ to investigate the changes in transcriptome and proteome of ‘Sanhu’ red tangerine roots following inoculation with HLB bacteria. Our results showed that HLB-infection changed significantly the expression of 3956 genes in roots, a number that is much larger than that obtained by microarray analysis [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>]. The vast discrepancy in DEG numbers should be related to the different sensitivities of the two methods: microarray is less sensitive since the hybridization signals of certain probes can be either saturated by over representative genes or too weak to be detected for rare transcripts [<xref rid="pone.0126973.ref033" ref-type="bibr">33</xref>]; in contrast, RNA-seq counts the absolute number of the transcripts and therefore the sensitivity can always be guaranteed by increasing sequencing coverage [<xref rid="pone.0126973.ref034" ref-type="bibr">34</xref>].</p><p>We also detected 78 differentially regulated proteins in this study. A moderate positive correlation was found between our DEP and DEG data, indicating HLB-induced changes in gene expression are regulated at both transcriptional and post-transcriptional levels. Given that our sampling date of 50 dpi was earlier than other previous transcriptomic researches [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>, <xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>–<xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>] and that it takes time for cells to mature mRNAs and to translate them, it may also be possible that the genes’ expression changes may have not yet led to a significant turnover in their protein levels at 50 dpi.</p><p>Comparison between our data and those obtain in other studies [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>, <xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>–<xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>] reveled that many common genes and hence the relevant pathways are regulated in both the above ground and the underground tissues (<xref rid="pone.0126973.t004" ref-type="table">Table 4</xref>). These pathways included the stress-response pathways that are up-regulated, the cell-wall modification pathways that are up-regulated, the photosynthesis pathway that is repressed except in fruits, the protease-mediated protein degradation pathway that is down-regulated, the cell cycle and cell division related genes that are mostly down-regulated, the zinc transporters that are up-regulated, the phloem proteins that are up-regulated in leaves and roots, among others. However, some responses of root-specific or opposite to those of the above ground tissues did exist as discussed in the following sections.</p><sec id="sec009"><title>HLB-infection reduced the overall defense capability in roots of the host</title><p>The most eye-catching changes were the down-regulation in terpenoid, flavonoid and phenylpropanoid biosynthesis pathways in roots following HLB infection since many of the pathways’ biosynthesis genes were down-regulated. Flavonoids are anti-fungi substances and antioxidants [<xref rid="pone.0126973.ref035" ref-type="bibr">35</xref>, <xref rid="pone.0126973.ref036" ref-type="bibr">36</xref>]. Phenylpropanoids serve as structural polymers including lignins, provide protection from pests and UV light and attract pollinators as pigments [<xref rid="pone.0126973.ref037" ref-type="bibr">37</xref>]. Important terpenoids include GA and ABA, carotenoids and some anti-pest chemicals [<xref rid="pone.0126973.ref038" ref-type="bibr">38</xref>]. Taken together, the defense of the root cells may be greatly weakened from a reduced biosynthesis of defensive substances in the host by HLB bacteria at the very early stage of their infection.</p><p>Plants use a diverse array of cytochrome P450 monooxygenases in biosynthesis of secondary metabolites and in detoxification [<xref rid="pone.0126973.ref039" ref-type="bibr">39</xref>]. It was shown in this study that most of the proteins’ genes were down-regulated, which may signal a reduced biosynthesis of secondary metabolites and a reduced reducing power in HLB-infected roots.</p><p>A notable finding in this study was that the negative regulator of plant defense against bacterial infection, <italic>RIN4</italic> [<xref rid="pone.0126973.ref040" ref-type="bibr">40</xref>], was up-regulated in HLB-infected roots at both 20 dpi and 50 dpi. RIN4 was shown to be associated with two NB-LRR immune receptors, RPS2 and RPM1, in planta [<xref rid="pone.0126973.ref041" ref-type="bibr">41</xref>, <xref rid="pone.0126973.ref042" ref-type="bibr">42</xref>]. It can be cleaved by avrRpt2 to activate RPS2-dependent resistance [<xref rid="pone.0126973.ref042" ref-type="bibr">42</xref>]. It can also be phosphorylated indirectly by avrB and avrRpm1 to activate RPM1 which in turn activates resistance responses [<xref rid="pone.0126973.ref040" ref-type="bibr">40</xref>]. The gene’s up-regulation indicated that HLB bacteria may harness the gene to facilitate their colonization.</p><p>PPRRPs constitute the largest protein super family in planta and are mostly located in organelles such as mitochondria and chloroplast [<xref rid="pone.0126973.ref043" ref-type="bibr">43</xref>–<xref rid="pone.0126973.ref045" ref-type="bibr">45</xref>]. The down-regulation in expression of a very large proportion of <italic>PPRRP</italic>s may indicate that a shortage in energy supply occurred in <italic>C</italic>Las-infected roots since PPRRPs are generally involved in proton-electron translocation in mitochondria. It may also indicate a decreased oxidative respiration that otherwise enhances stress tolerance [<xref rid="pone.0126973.ref045" ref-type="bibr">45</xref>, <xref rid="pone.0126973.ref046" ref-type="bibr">46</xref>].</p></sec><sec id="sec010"><title>HLB-infection reduced greatly the absorption of N, P, Zn and Fe</title><p>As roots are the sole organ to absorb and supply inorganic nutrients for the whole tree, the nutrient deficiencies in leaves should be closely related to the function of roots. It was reported that zinc and phosphorus content was significantly reduced in HLB infected trees [<xref rid="pone.0126973.ref014" ref-type="bibr">14</xref>, <xref rid="pone.0126973.ref025" ref-type="bibr">25</xref>] and that Zn deficiency induced the expression of genes encoding phosphate transporters in barley roots [<xref rid="pone.0126973.ref047" ref-type="bibr">47</xref>]. Our study showed that zinc and phosphate transporter genes were similarly up-regulated in roots as in leaves and stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>, <xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>]. Whether this up-regulation is resulted from zinc or/and phosphorus deficiency requires further investigation. Two nitrate transporter genes, <italic>NRT1</italic> and <italic>NRT1</italic>:<italic>2</italic> were reported to be up-regulated in stems [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>] but our result showed <italic>NRT2</italic>:<italic>1</italic> and <italic>NRT2</italic>:<italic>5</italic> were down-regulated in roots. Apparently, HLB infected trees are deficient in nitrogen, which accounts largely for the characteristic chlorosis symptom [<xref rid="pone.0126973.ref015" ref-type="bibr">15</xref>]. And a down-regulation in nitrogen transporter genes in roots strongly indicated a reduced supply of the element to the above ground tissues. Fe is essential for photosynthesis and chlorophyll synthesis, and deficiency in Fe results in leaf chlorosis. Fe as cofactor is also necessary for some enzymes to function normally. It was reported that Fe in some HLB-infected citrus genotypes was only half of the level of the healthy plants, indicating that Fe homeostasis is significantly affected during infection [<xref rid="pone.0126973.ref014" ref-type="bibr">14</xref>]. In our study 3 genes encoding FRO2, FRO7 and FRO8 were all down-regulated by <italic>C</italic>Las-infection, strongly suggesting that the normal Fe absorption and transportation are impaired in roots for these ferric chelate reductases are responsible for reducing insoluble Fe<sup>3+</sup> to soluble Fe<sup>2+</sup> [<xref rid="pone.0126973.ref048" ref-type="bibr">48</xref>]. Clearly, our data can explain, at least in part, for the leaf chlorosis symptom associated with HLB infection.</p></sec><sec id="sec011"><title>HLB-infection can nevertheless induce some defense responses</title><p>Phloem protein 2 (PP2) participates in the formation of high-molecular-weight polymers that plug the sieve plate pores of injured sieve tube elements [<xref rid="pone.0126973.ref049" ref-type="bibr">49</xref>, <xref rid="pone.0126973.ref050" ref-type="bibr">50</xref>], and shows also <italic>in vitro</italic> [<xref rid="pone.0126973.ref051" ref-type="bibr">51</xref>] as well as <italic>in vivo</italic> [<xref rid="pone.0126973.ref052" ref-type="bibr">52</xref>] insecticidal activities. <italic>PP2-like protein</italic> genes were reported in HLB-infected leaves [<xref rid="pone.0126973.ref016" ref-type="bibr">16</xref>–<xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>]. We also identified a strong up-regulation in the expression of 6 <italic>PP2-like</italic> genes in roots. Our qRT-PCR result confirmed that the <italic>PP2-B15</italic> gene was induced quickly at 20 dpi and more significantly at 50 dpi. It therefore seemed that the increased expression in many <italic>PP2-like</italic> genes following <italic>C</italic>Las infection has an active role in defense against the invading bacteria and perhaps even the feeding psyllids. Previous studies indeed proposed that these proteins were responsible for the widely observed callose deposition in the infected sieve tube elements in leaves [<xref rid="pone.0126973.ref009" ref-type="bibr">9</xref>, <xref rid="pone.0126973.ref018" ref-type="bibr">18</xref>]. However, <italic>GSL7</italic>, a callose synthase gene that is necessary for normal phloem carbohydrate transport and inflorescence growth [<xref rid="pone.0126973.ref029" ref-type="bibr">29</xref>], was down-regulated in HLB-infected roots as shown in this study (<xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref>), possibly signifying a reduced transport of assimilates in the infected phloem tube elements, which might be result in carbohydrate starvation as shown in the <italic>Arabidopsis</italic> mutant <italic>gsl7</italic>. Interestingly, the expression of <italic>βGlu</italic>, whose products hydrolyze callose [<xref rid="pone.0126973.ref053" ref-type="bibr">53</xref>], was up-regulated by <italic>C</italic>Las-infection (<xref rid="pone.0126973.t002" ref-type="table">Table 2</xref>), indicating again a disturbed callose lining of the sieve plate pores that is required for normal carbohydrate transportation. The contradictory regulation in callose synthesis and degradation genes may indicate that cells are hanging between victory and defeat in their fight against <italic>C</italic>las at this stage.</p><p>Of the dozens of <italic>UGT</italic> DEGs that were significantly regulated in <italic>C</italic>Las-infected roots, more were down-regulated than up-regulated (<xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref>). But the few <italic>UGT</italic>s detected in HLB-infected above ground tissues were mostly up-regulated [<xref rid="pone.0126973.ref018" ref-type="bibr">18</xref>, <xref rid="pone.0126973.ref021" ref-type="bibr">21</xref>, <xref rid="pone.0126973.ref024" ref-type="bibr">24</xref>]. The exact role of these UGTs in response of citrus to <italic>C</italic>Las-infection is not clear since knocking out certain <italic>UGTs</italic> enhanced defense against <italic>Pseudomonas syringae</italic> but knocking out some other <italic>UGTs</italic> increased susceptibility to the same bacterium in <italic>Arabidopsis</italic> [<xref rid="pone.0126973.ref054" ref-type="bibr">54</xref>, <xref rid="pone.0126973.ref055" ref-type="bibr">55</xref>].</p><p>SA signaling pathway may be activated in <italic>C</italic>Las-infected roots since the key SA signaling-related gene <italic>NPR1</italic> (ciclev10031627m) was up-regulated and one of the pathway’s downstream genes [<xref rid="pone.0126973.ref056" ref-type="bibr">56</xref>], <italic>PR1</italic>, was concomitantly up-regulated. Further more, 2 PR proteins, PR3 and PR4, were also up-regulated. <italic>ALD1</italic>, a gene that was reported to be activated by SA, was up-regulated [<xref rid="pone.0126973.ref057" ref-type="bibr">57</xref>]. In addition, several <italic>WRKY transcription factor</italic> genes that participate in SA- and JA- dependent defense pathways were up-regulated [<xref rid="pone.0126973.ref058" ref-type="bibr">58</xref>].</p><p>Proteolysis is fundamental for the normal functioning of multicellular organisms and plays key roles in a variety of biological processes including defense and stress responses [<xref rid="pone.0126973.ref059" ref-type="bibr">59</xref>]. Recently, the possible role of subtilisin-like protease, a serine protease, in plant-pathogen recognition and immune priming has been suggested [<xref rid="pone.0126973.ref060" ref-type="bibr">60</xref>]. CDR1, a secreted aspartic protease, was also reported to function in plant defense responses [<xref rid="pone.0126973.ref061" ref-type="bibr">61</xref>]. Aspartic and cysteine proteases were demonstrated to be associated with defense [<xref rid="pone.0126973.ref062" ref-type="bibr">62</xref>, <xref rid="pone.0126973.ref063" ref-type="bibr">63</xref>]. Therefore it was not surprising to find that the genes of these proteases were regulated in HLB-infected roots (<xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref> and <xref rid="pone.0126973.t002" ref-type="table">Table 2</xref>). The surprise was, however, that some of their corresponding proteins were elevated to a level that was high enough to allow them to be identified as of the mere 78 DEPs. But the ubiquitin-dependent protein degradation pathway, as discussed in above, was down-regulated in HLB-infected roots. In this respect, it was known that some pathogens have acquired during evolution the ability to subvert the host’s proteasomal degradation pathway to facilitate their infection [<xref rid="pone.0126973.ref064" ref-type="bibr">64</xref>], suggesting that <italic>C</italic>Las may have also evolved the same strategy to counteract the attacks of its hosts.</p><p>Several other genes (and their encoded proteins) that were highly up-regulated in <italic>C</italic>Las-infected ‘Sanhu’ red tangerine roots (<xref rid="pone.0126973.t002" ref-type="table">Table 2</xref>) included several <italic>germin-like proteins</italic> and 1 <italic>SCPL40</italic>. Germins and germin-like proteins could be induced in the resistance response of plants to bacterial infections [<xref rid="pone.0126973.ref065" ref-type="bibr">65</xref>]. SCPLs have recently emerged as a new group of plant acyltransferases that are required for the synthesis of antimicrobial compounds [<xref rid="pone.0126973.ref066" ref-type="bibr">66</xref>, <xref rid="pone.0126973.ref067" ref-type="bibr">67</xref>]. The facts that the highest and the second highest up-regulated proteins were SSP411 and the copper ion binding protein in HLB-infected roots (<xref rid="pone.0126973.t002" ref-type="table">Table 2</xref>) strongly suggested that the proteins play some important roles in the response of citrus to <italic>C</italic>Las-infection.</p></sec></sec><sec sec-type="materials|methods" id="sec012"><title>Materials and Methods</title><sec id="sec013"><title>Plant materials and treatments</title><p>Two-year-old seedlings of ‘Sanhu’ red tangerine were grafted with buds from <italic>C</italic>Las-infected or <italic>C</italic>Las-free ‘Gonggan’ mandarin trees. Mature leaves and roots were collected from the <italic>C</italic>Las-inoculated and the control trees every ten days to detect for <italic>C</italic>Las by PCR. DNA used for PCR was extracted with the use of the Plant DNA isolation Kit (Trans, Beijing, China) according to manufacturer’s instructions. Primers used for <italic>C</italic>Las detection were the same A2/J5 as reported by Hocquellet <italic>et al</italic>. [<xref rid="pone.0126973.ref068" ref-type="bibr">68</xref>].</p></sec><sec id="sec014"><title>RNA-sequencing and iTRAQ analysis</title><p>The fibrous roots of 3 <italic>C</italic>Las-positive and 3 control <italic>C</italic>Las-free trees were individually collected at 50 dpi when the HLB-inoculated trees became <italic>C</italic>Las-positive in both leaves and roots yet showed no visible chlorosis and other HLB symptoms. This should have allowed us not to miss too many early responsive genes but at the same time ensured that the trees were infected as expected. Total RNA was extracted from each sample using RNeasy plant mini kit (Qiagen, Valencia, CA) and further purified using the RQ1 Rnase Free Dnase Kit (Promega, Madison, USA). RNA quality and quantity were assessed by gel-electrophoresis and by absorbance at OD260/OD280, respectively. Aliquot RNA samples were stored at -80°C. For RNA-seq analysis, RNA samples from the three trees were mixed in equal amount and used for cDNA library construction following the Illumina mRNA-sequencing sample preparation protocol (Illumina, San Diego, CA). The 90-bp raw paired end reads were generated by Illumina HiSeq 2000. The RNA-Seq data have been submitted to the Gene Expression Omnibus (GEO) database (<ext-link ext-link-type="uri" xlink:href="http://www.ncbi.nlm.nih.gov/geo/info/linking.html">http://www.ncbi.nlm.nih.gov/geo/info/linking.html</ext-link>.); Accession number GSE67560.</p><p>Total proteins were also extracted from the same samples and subject to iTRAQ labeling, SCX chromatography fractionation and LC-ESI-MS/MS analysis with the same method as described by Yang <italic>et al</italic>. [<xref rid="pone.0126973.ref069" ref-type="bibr">69</xref>].</p></sec><sec id="sec015"><title>Data analysis</title><p>RNA-sequencing data were filtered to remove low quality reads. The clean individual reads from both the <italic>C</italic>Las infected and the control libraries were aligned first to the <italic>C</italic>. <italic>clementina</italic> genome and then to all transcript sequences (<ext-link ext-link-type="uri" xlink:href="http://www.phytozome.org">http://www.phytozome.org</ext-link>.) in 2011 with a mismatch penalty of no more than 1 nucleotide. For quantitative gene expression analysis, the transcripts of each gene were normalized to RMPK (reads per kb per million reads) and the DEGs were further annotated using Blast2GO and MapMan [<xref rid="pone.0126973.ref070" ref-type="bibr">70</xref>, <xref rid="pone.0126973.ref071" ref-type="bibr">71</xref>], and the MapMan results were shown in <xref rid="pone.0126973.s002" ref-type="supplementary-material">S1 Table</xref>.</p><p>Raw iTRAQ data files acquired from the Orbitrap were converted into MGF files using Proteome Discoverer 1.2 (PD 1.2, Thermo). Subsequent database searches were carried out by Mascot Daemon (version 2.3.02, Matrix Science, Boston, MA) for both protein identification and iTRAQ quantification against the <italic>C</italic>. <italic>clementina</italic> (Cclementina_165). The quantitative protein ratios were weighted and normalized by the median ratio with outlier removal in Mascot in which the imbedded isotope correction factors were applied. Proteins with a ≥ ∣±1.5∣-fold change (<italic>C</italic>Las-infected vs. control) were defined as differentially expressed proteins (DEPs). The functional annotation and classification of all DEPs were performed by using Blast2GO and MapMan and the MapMan results were summarized in <xref rid="pone.0126973.s003" ref-type="supplementary-material">S2 Table</xref>.</p><p>To identify and to provide a statistics-based overview of the changed pathways, the DEGs and DEPs were analyzed by PageMan embedded in MapMan. The Wilcoxon test was applied and the Benjamini and Hochberg approach corrected p-value (<0.05) were generated [<xref rid="pone.0126973.ref072" ref-type="bibr">72</xref>]. Pearson method was used to analyze the correlation between the levels of DEPs and those of their corresponding mRNAs.</p></sec><sec id="sec016"><title>Quantitative real time PCR</title><p>Reverse transcription was performed using total RNA from each biological replicates as template using the PrimeScript RT reagent Kit with gDNA Eraser (Perfect Real Time) (Takara, Dalian, China) according to the manufacturer’s instruction. The 16 genes selected include 11 up-regulated genes (two <italic>RPM1 interacting protein 4</italic> (<italic>RIN4</italic>), <italic>invertase</italic>, <italic>Phloem protein 2-B15</italic> (<italic>PP2-B15</italic>), <italic>NPR1 regulatory protein (NPR1)</italic>, <italic>trehalose-phosphate phosphatase-like (TPP)</italic>, <italic>act repeat 4</italic> (ACR4), <italic>disease resistant protein ribosomal protein S2</italic> (<italic>RPS2</italic>), <italic>disease resistance protein TIR-NBS-LRR class (DPI)</italic>, <italic>cysteine-rich protein kinase</italic> (<italic>CRPK</italic>), <italic>xyloglucan endotransglucosylase hydrolase</italic> (<italic>XTR6</italic>)) and 5 down-regulated genes (<italic>bri1 kinase inhibitor 1</italic> (BRI1), <italic>bzip transcription protein factor-like</italic> (BZIP), <italic>3-ketoacyl-CoA synthase 6</italic> (<italic>KCS6</italic>), <italic>β-amylase</italic> (BAM) and <italic>pectin methylesterase inhibitor</italic> (<italic>PMEI</italic>)) identified by RNA-seq. qRT-PCR was carried out in Lightcycler 480II (Roche, Switzerland) using SYBR Green real time PCR Master Mix (Toyobo, Osaka, Japan) according to Cheng <italic>et al</italic>. [<xref rid="pone.0126973.ref073" ref-type="bibr">73</xref>]. <italic>Actin</italic> gene was used as the endogenous control. The expression was calculated by 2<sup>-ΔΔCt</sup> and normalized against <italic>actin</italic> gene expression level. Genes analyzed and their primers used were listed in <xref rid="pone.0126973.s004" ref-type="supplementary-material">S3 Table</xref>.</p></sec></sec><sec sec-type="supplementary-material" id="sec017"><title>Supporting Information</title><supplementary-material content-type="local-data" id="pone.0126973.s001"><label>S1 Fig</label><caption><title>Pearson correlation analysis result between DEGs and DEPs in HLB infected roots.</title><p>(TIF)</p></caption><media xlink:href="pone.0126973.s001.tif"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0126973.s002"><label>S1 Table</label><caption><title>Mapman analysis results of the differentially expressed genes in HLB-infected roots in comparison with control roots.</title><p>(XLS)</p></caption><media xlink:href="pone.0126973.s002.xls"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0126973.s003"><label>S2 Table</label><caption><title>Mapman analysis results of the differentially expressed proteins in HLB-infected roots in comparison with control roots.</title><p>(XLS)</p></caption><media xlink:href="pone.0126973.s003.xls"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0126973.s004"><label>S3 Table</label><caption><title>Primers for real time PCR analysis.</title><p>(DOCX)</p></caption><media xlink:href="pone.0126973.s004.docx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec></body><back><ref-list><title>References</title><ref id="pone.0126973.ref001"><label>1</label><mixed-citation publication-type="journal"><name><surname>Batool</surname><given-names>A</given-names></name>, <name><surname>Iftikhar</surname><given-names>Y</given-names></name>, <name><surname>Mughal</surname><given-names>SM</given-names></name>, <name><surname>Khan</surname><given-names>MM</given-names></name>, <name><surname>Jaskani</surname><given-names>MJ</given-names></name>, <name><surname>Abbas</surname><given-names>M</given-names></name>, <etal>et al</etal><article-title>Citrus greening disease—A major cause of citrus decline in the world—A Review</article-title>. <source>Hort Sci (Prague)</source>. <year>2007</year>;<volume>34</volume>: <fpage>159</fpage>–<lpage>166</lpage>.</mixed-citation></ref><ref id="pone.0126973.ref002"><label>2</label><mixed-citation publication-type="journal"><name><surname>Román</surname><given-names>MP</given-names></name>, <name><surname>Cambra</surname><given-names>M</given-names></name>, <name><surname>Juárez</surname><given-names>J</given-names></name>, <name><surname>Moreno</surname><given-names>P</given-names></name>, <name><surname>Duran-Vila</surname><given-names>N</given-names></name>, <name><surname>Tanaka</surname><given-names>FAO</given-names></name>, <etal>et al</etal><article-title>Sudden death of citrus in Brazil: A graft-transmissible bud union disease</article-title>. <source>Plant Dis</source>. <year>2004</year>;<volume>88</volume>: <fpage>453</fpage>–<lpage>467</lpage>.</mixed-citation></ref><ref id="pone.0126973.ref003"><label>3</label><mixed-citation publication-type="journal"><name><surname>Bové</surname><given-names>JM</given-names></name>. <article-title>Huanglongbing: A destructive, newly-emerging, century-old disease of citrus</article-title>. <source>J Plant Pathol</source>. <year>2006</year>;<volume>88</volume>: <fpage>7</fpage>–<lpage>37</lpage>.</mixed-citation></ref><ref id="pone.0126973.ref004"><label>4</label><mixed-citation publication-type="journal"><name><surname>Coletta-Filho</surname><given-names>HDC</given-names></name>, <name><surname>Takita</surname><given-names>MA</given-names></name>, <name><surname>Targon</surname><given-names>MLPN</given-names></name>, <name><surname>Machado</surname><given-names>MA</given-names></name>. <article-title>Analysis of 16S rDNA sequences from citrus Huanglongbing bacteria reveal a different ‘<italic>Ca</italic>. 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