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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Digital Gene Expression Analysis of Ponkan Mandarin (<italic>Citrus reticulata</italic>
Blanco) in Response to Asia Citrus Psyllid-Vectored Huanglongbing Infection</title>
<author><name sortKey="Zhong, Yun" sort="Zhong, Yun" uniqKey="Zhong Y" first="Yun" last="Zhong">Yun Zhong</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cheng, Chunzhen" sort="Cheng, Chunzhen" uniqKey="Cheng C" first="Chunzhen" last="Cheng">Chunzhen Cheng</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af2-ijms-17-01063">Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China;<email>zhyy0425@126.com</email>
</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="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Jiang, Nonghui" sort="Jiang, Nonghui" uniqKey="Jiang N" first="Nonghui" last="Jiang">Nonghui Jiang</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhang, Yongyan" sort="Zhang, Yongyan" uniqKey="Zhang Y" first="Yongyan" last="Zhang">Yongyan Zhang</name>
<affiliation><nlm:aff id="af2-ijms-17-01063">Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China;<email>zhyy0425@126.com</email>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hu, Minlun" sort="Hu, Minlun" uniqKey="Hu M" first="Minlun" last="Hu">Minlun Hu</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhong, Guangyan" sort="Zhong, Guangyan" uniqKey="Zhong G" first="Guangyan" last="Zhong">Guangyan Zhong</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">27384559</idno>
<idno type="pmc">4964439</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4964439</idno>
<idno type="RBID">PMC:4964439</idno>
<idno type="doi">10.3390/ijms17071063</idno>
<date when="2016">2016</date>
<idno type="wicri:Area/Pmc/Corpus">000348</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Digital Gene Expression Analysis of Ponkan Mandarin (<italic>Citrus reticulata</italic>
Blanco) in Response to Asia Citrus Psyllid-Vectored Huanglongbing Infection</title>
<author><name sortKey="Zhong, Yun" sort="Zhong, Yun" uniqKey="Zhong Y" first="Yun" last="Zhong">Yun Zhong</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Cheng, Chunzhen" sort="Cheng, Chunzhen" uniqKey="Cheng C" first="Chunzhen" last="Cheng">Chunzhen Cheng</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af2-ijms-17-01063">Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China;<email>zhyy0425@126.com</email>
</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="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Jiang, Nonghui" sort="Jiang, Nonghui" uniqKey="Jiang N" first="Nonghui" last="Jiang">Nonghui Jiang</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhang, Yongyan" sort="Zhang, Yongyan" uniqKey="Zhang Y" first="Yongyan" last="Zhang">Yongyan Zhang</name>
<affiliation><nlm:aff id="af2-ijms-17-01063">Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China;<email>zhyy0425@126.com</email>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Hu, Minlun" sort="Hu, Minlun" uniqKey="Hu M" first="Minlun" last="Hu">Minlun Hu</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhong, Guangyan" sort="Zhong, Guangyan" uniqKey="Zhong G" first="Guangyan" last="Zhong">Guangyan Zhong</name>
<affiliation><nlm:aff id="af1-ijms-17-01063">Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="af3-ijms-17-01063">Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">International Journal of Molecular Sciences</title>
<idno type="eISSN">1422-0067</idno>
<imprint><date when="2016">2016</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Citrus Huanglongbing (HLB), the most destructive citrus disease, can be transmitted by psyllids and diseased budwoods. Although the final symptoms of the two main HLB transmission ways were similar and hard to distinguish, the host responses might be different. In this study, the global gene changes in leaves of ponkan (<italic>Citrus reticulata</italic>
) mandarin trees following psyllid-transmission of HLB were analyzed at the early symptomatic stage (13 weeks post inoculation, wpi) and late symptomatic stage (26 wpi) using digital gene expression (DGE) profiling. At 13 wpi, 2452 genes were downregulated while only 604 genes were upregulated in HLB infected ponkan leaves but no pathway enrichment was identified. Gene function analysis showed impairment in defense at the early stage of infection. At late stage of 26 wpi, however, differentially expressed genes (DEGs) involved in carbohydrate metabolism, plant defense, hormone signaling, secondary metabolism, transcription regulation were overwhelmingly upregulated, indicating that the defense reactions were eventually activated. The results indicated that HLB bacterial infection significantly influenced ponkan gene expression, and a delayed response of the host to the fast growing bacteria might be responsible for its failure in fighting against the bacteria.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Mol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijms</journal-id>
<journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1422-0067</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27384559</article-id>
<article-id pub-id-type="pmc">4964439</article-id>
<article-id pub-id-type="doi">10.3390/ijms17071063</article-id>
<article-id pub-id-type="publisher-id">ijms-17-01063</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Digital Gene Expression Analysis of Ponkan Mandarin (<italic>Citrus reticulata</italic>
Blanco) in Response to Asia Citrus Psyllid-Vectored Huanglongbing Infection</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Zhong</surname>
<given-names>Yun</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-17-01063">1</xref>
<xref ref-type="author-notes" rid="fn1-ijms-17-01063">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cheng</surname>
<given-names>Chunzhen</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-17-01063">1</xref>
<xref ref-type="aff" rid="af2-ijms-17-01063">2</xref>
<xref ref-type="author-notes" rid="fn1-ijms-17-01063">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jiang</surname>
<given-names>Bo</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-17-01063">1</xref>
<xref ref-type="aff" rid="af3-ijms-17-01063">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jiang</surname>
<given-names>Nonghui</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-17-01063">1</xref>
<xref ref-type="aff" rid="af3-ijms-17-01063">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Yongyan</given-names>
</name>
<xref ref-type="aff" rid="af2-ijms-17-01063">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hu</surname>
<given-names>Minlun</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-17-01063">1</xref>
<xref ref-type="aff" rid="af3-ijms-17-01063">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhong</surname>
<given-names>Guangyan</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-17-01063">1</xref>
<xref ref-type="aff" rid="af3-ijms-17-01063">3</xref>
<xref rid="c1-ijms-17-01063" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Iriti</surname>
<given-names>Marcello</given-names>
</name>
<role>Academic Editor</role>
</contrib>
</contrib-group>
<aff id="af1-ijms-17-01063"><label>1</label>
Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China;<email>zhongyun99cn@163.com</email>
(Y.Z.);<email>ld0532cheng@126.com</email>
(C.C.);<email>jb-clinnic@webmail.hzau.edu.cn</email>
(B.J.);<email>jiangnonghui2002@163.com</email>
(N.J.);<email>fanshu2005@163.com</email>
(M.H.)</aff>
<aff id="af2-ijms-17-01063"><label>2</label>
Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China;<email>zhyy0425@126.com</email>
</aff>
<aff id="af3-ijms-17-01063"><label>3</label>
Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization Ministry of Agriculture, Guangzhou 510640, China</aff>
<author-notes><corresp id="c1-ijms-17-01063"><label>*</label>
Correspondence: <email>gy_zhong@163.com</email>
; Tel.: +86-20-3876-5087</corresp>
<fn id="fn1-ijms-17-01063"><label>†</label>
<p>These authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>02</day>
<month>7</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><month>7</month>
<year>2016</year>
</pub-date>
<volume>17</volume>
<issue>7</issue>
<elocation-id>1063</elocation-id>
<history><date date-type="received"><day>03</day>
<month>3</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>27</day>
<month>6</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 by the authors; licensee MDPI, Basel, Switzerland.</copyright-statement>
<copyright-year>2016</copyright-year>
<license><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>
This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>Citrus Huanglongbing (HLB), the most destructive citrus disease, can be transmitted by psyllids and diseased budwoods. Although the final symptoms of the two main HLB transmission ways were similar and hard to distinguish, the host responses might be different. In this study, the global gene changes in leaves of ponkan (<italic>Citrus reticulata</italic>
) mandarin trees following psyllid-transmission of HLB were analyzed at the early symptomatic stage (13 weeks post inoculation, wpi) and late symptomatic stage (26 wpi) using digital gene expression (DGE) profiling. At 13 wpi, 2452 genes were downregulated while only 604 genes were upregulated in HLB infected ponkan leaves but no pathway enrichment was identified. Gene function analysis showed impairment in defense at the early stage of infection. At late stage of 26 wpi, however, differentially expressed genes (DEGs) involved in carbohydrate metabolism, plant defense, hormone signaling, secondary metabolism, transcription regulation were overwhelmingly upregulated, indicating that the defense reactions were eventually activated. The results indicated that HLB bacterial infection significantly influenced ponkan gene expression, and a delayed response of the host to the fast growing bacteria might be responsible for its failure in fighting against the bacteria.</p>
</abstract>
<kwd-group><kwd>Asian citrus psyllids (ACP)</kwd>
<kwd>Citrus Huanglongbing (HLB)</kwd>
<kwd>ponkan mandarin</kwd>
<kwd>differentially expressed genes (DEGs)</kwd>
<kwd>digital gene expression (DGE)</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec id="sec1-ijms-17-01063"><title>1. Introduction</title>
<p>Citrus Huanglongbing (HLB), the most destructive citrus disease, can infect all citrus species, cultivars and hybrids, as well as some citrus relatives. Although the disease has been reported for about 100 years, neither HLB resistant rootstocks and citrus germplasm resources nor effective and durable HLB control methods have so far been explored except the common strategies of removing infected trees, using disease-free nursery trees, and applying an aggressive control program in the management of the vector insect [<xref rid="B1-ijms-17-01063" ref-type="bibr">1</xref>
,<xref rid="B2-ijms-17-01063" ref-type="bibr">2</xref>
,<xref rid="B3-ijms-17-01063" ref-type="bibr">3</xref>
].</p>
<p>The HLB disease is associated with a phloem-limited <italic>α-proteobacterium</italic>
designated as <italic>Candidatus</italic>
Liberibacter (<italic>Ca</italic>
). So far, three forms of <italic>Ca.</italic>
Liberibacters, i.e., the Asian form <italic>Ca.</italic>
L. asiaticus (<italic>C</italic>
Las), the American form <italic>Ca.</italic>
L. americanus (<italic>C</italic>
Lam) and the African form <italic>Ca.</italic>
L. africanus (<italic>C</italic>
Laf), have been identified [<xref rid="B2-ijms-17-01063" ref-type="bibr">2</xref>
], and the <italic>C</italic>
Las is the most widespread and severe one. <italic>C</italic>
Las and <italic>C</italic>
Lam are transmitted by the Asian citrus psyllid (ACP), <italic>Diaphorina</italic>
<italic>citri</italic>
Kuwayama, while the <italic>C</italic>
Laf is transmitted by the African citrus psyllid, <italic>Trioza</italic>
<italic>erytrea</italic>
Del Guercio. HLB bacteria could also be transmitted by dodders or by grafting with infected budwoods [<xref rid="B4-ijms-17-01063" ref-type="bibr">4</xref>
]. Once the plant is colonized, HLB bacteria are restricted to the phloem of the host. The phloem is the main traffic route for vital metabolites including carbohydrates, defensive compounds and signaling molecules. Interruption in the transport of these molecules becomes inevitable as the bacteria spread [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
]. Nutrient deficiencies and carbohydrate metabolism changes were reported by several studies [<xref rid="B6-ijms-17-01063" ref-type="bibr">6</xref>
,<xref rid="B7-ijms-17-01063" ref-type="bibr">7</xref>
]. Nutrient deficiency is found to be one of the typical leaf symptoms in addition to yellowing and asymmetric blotchy mottling [<xref rid="B2-ijms-17-01063" ref-type="bibr">2</xref>
,<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
]. Many anatomical disorders such as starch accumulation, callose deposition, phloem plugging and collapse, swelling of sieve element and companion cell walls, and disruption of chloroplast inner grana structures have been observed in HLB infected leaves [<xref rid="B2-ijms-17-01063" ref-type="bibr">2</xref>
,<xref rid="B7-ijms-17-01063" ref-type="bibr">7</xref>
,<xref rid="B8-ijms-17-01063" ref-type="bibr">8</xref>
,<xref rid="B9-ijms-17-01063" ref-type="bibr">9</xref>
,<xref rid="B10-ijms-17-01063" ref-type="bibr">10</xref>
,<xref rid="B11-ijms-17-01063" ref-type="bibr">11</xref>
].</p>
<p>Disease symptom development is considered to be the consequence of molecular, cellular, and physiological changes in the interaction of the host plant with the invading pathogen [<xref rid="B12-ijms-17-01063" ref-type="bibr">12</xref>
], and understanding the host responses to pathogen infection at a molecular level is therefore very necessary for the clarification of the plant–microbe interaction mechanisms and for the development of novel disease control strategies [<xref rid="B13-ijms-17-01063" ref-type="bibr">13</xref>
]. In this regard, several studies have been performed on the global gene expression changes in citrus leaves [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
,<xref rid="B8-ijms-17-01063" ref-type="bibr">8</xref>
,<xref rid="B13-ijms-17-01063" ref-type="bibr">13</xref>
,<xref rid="B14-ijms-17-01063" ref-type="bibr">14</xref>
,<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
,<xref rid="B16-ijms-17-01063" ref-type="bibr">16</xref>
,<xref rid="B17-ijms-17-01063" ref-type="bibr">17</xref>
], fruits [<xref rid="B18-ijms-17-01063" ref-type="bibr">18</xref>
,<xref rid="B19-ijms-17-01063" ref-type="bibr">19</xref>
], stems and roots [<xref rid="B20-ijms-17-01063" ref-type="bibr">20</xref>
,<xref rid="B21-ijms-17-01063" ref-type="bibr">21</xref>
], and some gene co-expression network analyses were also conducted to identify candidate citrus genes with potentials of against HLB [<xref rid="B22-ijms-17-01063" ref-type="bibr">22</xref>
,<xref rid="B23-ijms-17-01063" ref-type="bibr">23</xref>
,<xref rid="B24-ijms-17-01063" ref-type="bibr">24</xref>
]. Though a substantial amount of knowledge has been generated, it should be noted that all the HLB-infected citrus trees used in the above studies were from grafting with HLB infected buds or from symptomatic trees in open field. However, the possibility cannot be ruled out that citrus might respond differently to psyllid transmitted and graft-transmitted HLB infections as bacteria titters could differ by more than 1000-fold [<xref rid="B25-ijms-17-01063" ref-type="bibr">25</xref>
] and times required for a successful transmission also differed a lot between the two transmission pathways [<xref rid="B26-ijms-17-01063" ref-type="bibr">26</xref>
]. It is, therefore, worth investigating ACP-vectored infection to better understand the HLB pathogenesis.</p>
<p>Ponkan is widely cultivated in Asian countries for its high quality fruits, but ponkan production has been problematic in HLB endemic areas since ponkan trees are highly susceptible to HLB infection. Knowledge about why ponkan trees collapse rapidly following HLB infection is also of great value to the understanding of HLB progression.</p>
<p>In the present study, a digital gene expression (DGE) profiling [<xref rid="B27-ijms-17-01063" ref-type="bibr">27</xref>
] was used to detect the changes in global gene expression in ponkan mandarin (<italic>C. reticulata</italic>
Blanco) leaves following exposing the trees to ACP adults raised on HLB symptomatic trees. The time-course transcriptional changes at the early symptomatic (13 weeks post inoculation, wpi) and symptomatic (26 wpi) stages of <italic>C</italic>
Las infection were compared and discussed.</p>
</sec>
<sec id="sec2-ijms-17-01063"><title>2. Results</title>
<sec id="sec2dot1-ijms-17-01063"><title>2.1. Development of Citrus Huanglongbing (HLB) Symptoms on Experimental Trees</title>
<p>Three of the five ponkan trees exposed to <italic>C</italic>
Las-carrying psyllids were detected to be HLB positive by conventional PCR since 3 wpi while all the controls were HLB negative during the whole experiments (<xref ref-type="app" rid="app1-ijms-17-01063">Figure S1</xref>
). At 13 wpi, blotchy mottling symptom began to appear on some leaves of trees, and at 26 wpi, some HLB positive plants displayed typical symptoms of asymmetrical blotchy mottling. Leaf samples for DGE analysis were then taken from both the <italic>C</italic>
Las treated and the control plants at the two time points.</p>
</sec>
<sec id="sec2dot2-ijms-17-01063"><title>2.2. Digital Gene Expression (DGE) Profiling Result</title>
<p>Between 3,587,092 and 3,704,176 raw reads were generated from the two time points of both treatments (<xref ref-type="table" rid="ijms-17-01063-t001">Table 1</xref>
). Approximately 69.59% to 78.09% of the total reads could be successfully mapped to <italic>Citrus clementina</italic>
genome, and 54.30% and 64.69% of the distinct tags were mapped to the archived gene sequences (<xref ref-type="table" rid="ijms-17-01063-t001">Table 1</xref>
).</p>
</sec>
<sec id="sec2dot3-ijms-17-01063"><title>2.3. Functional Analysis of DGE Profiling Data</title>
<p>In total, 3056 and 2522 DEGs with fold change ≥1.5 (<italic>p</italic>
-value ≤ 0.005 and FDR (false discovery rate) ≤ 0.001) were identified to be regulated at 13 and 26 wpi, respectively. For the 3056 DEGs identified from samples at 13 wpi, 604 were upregulated whereas 2452 were downregulated (<xref ref-type="app" rid="app1-ijms-17-01063">Table S1</xref>
). For the 2522 DEGs identified from samples at 26 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S2</xref>
), 1759 were upregulated while 763 were downregulated. Only 585 DEGs were commonly identified from both time points (<xref ref-type="fig" rid="ijms-17-01063-f001">Figure 1</xref>
and <xref ref-type="app" rid="app1-ijms-17-01063">Table S3</xref>
).</p>
</sec>
<sec id="sec2dot4-ijms-17-01063"><title>2.4. Gene Pathway Enrichment Analysis of HLB-Modulated Pathways</title>
<p>PageMan analysis showed that no significantly changed pathway was identified at <italic>p</italic>
-value ≤0.05, although more DEGs were found at 13 wpi. The HLB significantly influenced 12 pathways at 26 wpi included protein synthesis, cell wall metabolism, transport, DNA synthesis, secondary metabolism, and auxin involved hormone signaling pathways etc. (<xref ref-type="table" rid="ijms-17-01063-t002">Table 2</xref>
). MapMan gene ontology results showed that these DEGs were mainly involved in diverse cellular functions including carbohydrate metabolism, stress-response-pathways, transport, cell organization, etc. (<xref ref-type="fig" rid="ijms-17-01063-f002">Figure 2</xref>
and <xref ref-type="fig" rid="ijms-17-01063-f003">Figure 3</xref>
).</p>
</sec>
<sec id="sec2dot5-ijms-17-01063"><title>2.5. Carbohydrate Metabolism Was Significantly Regulated by HLB Infection</title>
<p>DEGs involved in carbohydrate metabolism were mostly downregulated at early infection stage (13 wpi) but mostly upregulated later at 26 wpi (<xref ref-type="fig" rid="ijms-17-01063-f002">Figure 2</xref>
). Two sucrose and starch related DEGs, <italic>sucrose-phosphate synthase</italic>
(<italic>SPS</italic>
) (ciclev10018655m) and <italic>β-fructofuranosidase/invertase</italic>
(ciclev10019134m), were found to be upregulated at both 13 and 26 wpi. Transcripts for 1 AGPase, 2 starch synthase, 1 sucrose-phosphatase 1 (SPP1), and 1 β-amylase were downregulated while other starch degradation related genes were all upregulated at 26 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S2</xref>
).</p>
<p>Notably, four raffinose metabolism related genes including two <italic>galactinol synthase 2</italic>
, one <italic>galactinol synthase 4</italic>
, and one <italic>galactinol-sucrose galactosyltransferase</italic>
, were all found to be significantly induced by HLB infection at 13 wpi. The two <italic>galactinol synthase 2</italic>
genes were both upregulated by more than three-fold. Moreover, upregulation of two raffinose biosynthesis related genes, <italic>galactinol synthase 4</italic>
(ciclev10032043m) and <italic>stachyose synthase precursor</italic>
(ciclev10004372m), were also found at 26 wpi.</p>
<p>At 13 wpi, two <italic>glucan synthases</italic>
were downregulated, while three <italic>glucan synthase</italic>
genes were upregulated at 26 wpi. Genes involved in trehalose, sugar alcohols, myo-inositol and galactose were all downregulated at 13 wpi but were mostly upregulated at 26 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Tables S1 and S2</xref>
).</p>
</sec>
<sec id="sec2dot6-ijms-17-01063"><title>2.6. Stressresponse-Related Genes</title>
<p>MapMan categorized 714 (23.36%) and 622 (24.66%) DEGs into the “stress-related” at 13 and 26 wpi (<xref ref-type="fig" rid="ijms-17-01063-f004">Figure 4</xref>
), respectively. Stress response-related pathways such as cell wall, proteolysis, secondary metabolites, signaling and transcription factors, hormone signaling and heat shock protein involved pathways, displayed differential responses in HLB-infected ponkan leaves.</p>
<p>Almost all the cell wall-related genes were initially downregulated at 13 wpi but upregulated later at 26 wpi. At 13 wpi, only 2 of the 10 <italic>pathogenesis-related</italic>
(<italic>PR</italic>
) <italic>proteins</italic>
were upregulated. At 26 wpi, however, 10 of the 12 <italic>PR</italic>
DEGs were upregulated, and notably two disease resistance protein genes (ciclev10024511m and ciclev10022439m) were found to be upregulated by 9.5-fold and 11.5-fold, respectively (<xref ref-type="app" rid="app1-ijms-17-01063">Tables S1 and S2</xref>
).</p>
<p>At 13 wpi, 10 of the 23 <italic>MYB transcription factor</italic>
DEGs were upregulated. <italic>LHY</italic>
(<italic>late elongated hypocotyl</italic>
, ciclev10018966m) and <italic>EPR1</italic>
(<italic>early-phytochrome responsive 1</italic>
, ciclev10020135m) were found to be upregulated by more than four-fold at 13 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S1</xref>
). At 26 wpi, more upregulated transcription factor genes were found in HLB infected samples. However, the same <italic>LHY</italic>
gene (ciclev10018966m) was downregulated about two-fold (<xref ref-type="app" rid="app1-ijms-17-01063">Table S2</xref>
).</p>
<p>The expression of secondary metabolism related genes involved in the metabolisms of flavonoids, phenylpropanoids and lignin, isoprenoids and alkaloids was mostly downregulated at 13 wpi but mostly upregulated at 26 wpi (<xref ref-type="fig" rid="ijms-17-01063-f002">Figure 2</xref>
). A wax metabolism related gene, <italic>WAX2/CER3</italic>
(ciclev10007738m), was upregulated more than two-fold at 13 wpi. However, three wax-related genes including two <italic>CER1</italic>
and one <italic>wax synthase-related</italic>
were downregulated at 26 wpi. A <italic>GGPS1</italic>
(<italic>geranylgeranyl pyrophosphate synthase 1</italic>
) was upregulated about 10-fold at 26 wpi. Two <italic>VTE2/HPT1</italic>
(<italic>homogentisate</italic>
<italic>phytyltransferase 1</italic>
) genes were found to be downregulated at 13 wpi. While at 26 wpi, a <italic>VTE2</italic>
(ciclev10008336m) was upregulated about eight-fold. The simple phenols metabolism pathway was found to be significantly altered by HLB infection at 26 wpi (<xref ref-type="table" rid="ijms-17-01063-t002">Table 2</xref>
). Two <italic>IRX12</italic>
(<italic>irregular xylem 12</italic>
) (ciclev10031134m and ciclev10011400m), 1 <italic>LAC11</italic>
(<italic>laccase 11</italic>
) and 2 <italic>LAC17</italic>
(<italic>laccase 17</italic>
) genes were significantly induced. The two <italic>IRX12</italic>
genes were both highly upregulated about 10-fold at 26 wpi, but one of them (ciclev10031134m) was downregulated more than eight-fold at 13 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S3</xref>
).</p>
<p>Significant transcriptional changes in response to <italic>C</italic>
Las infection were observed for a group of genes involved in hormone biosynthesis and signaling (<xref ref-type="fig" rid="ijms-17-01063-f003">Figure 3</xref>
). At 13 wpi, most of the hormone-related genes were repressed by HLB infection. However, a gene of 2-oxoglutarate (<italic>2OG</italic>
) and Fe(II)-independent oxygenase (<italic>2OG-Fe(II) oxygenase</italic>
) was found to be upregulated by more than 11-fold (<xref ref-type="app" rid="app1-ijms-17-01063">Table S1</xref>
). Moreover, three jasmonic acid(JA) synthesis related <italic>lipoxygenase</italic>
genes were upregulated at 13 wpi. Auxin metabolism was found to be significantly modulated by HLB infection at 26 wpi with most of the involved genes upregulated. Ethylene and JA related DEGs were mostly upregulated at 26 wpi.</p>
<p>Signaling related DEGs encoding receptor like kinases (RLK), calcium modulating proteins and G-proteins were mainly downregulated at 13 wpi but upregulated at 26 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S3</xref>
). However, 3 <italic>RLK</italic>
genes were upregulated by more than 8-fold at 13 wpi.</p>
<p>Protein synthesis related genes were overwhelmingly repressed by HLB infection at both 13 and 26 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S3</xref>
). The expression of many <italic>heat shock proteins</italic>
was suppressed at 13 wpi, while several <italic>HSP70</italic>
genes were found to be upregulated at both 13 and 26 wpi.</p>
</sec>
<sec id="sec2dot7-ijms-17-01063"><title>2.7. Transport Related Genes Regulated by HLB Infection</title>
<p>One hundred and twenty eight and 126 transport related DEGs were identified in HLB infected ponkan at 13 and 26 wpi, respectively (<xref ref-type="fig" rid="ijms-17-01063-f004">Figure 4</xref>
, <xref ref-type="app" rid="app1-ijms-17-01063">Tables S1 and S2</xref>
). Most of the DEGs were downregulated at 13 wpi but induced at 26 wpi, but 4 <italic>PIP</italic>
s (<italic>plasma membrane intrinsic protein</italic>
) were upregulated at 13 wpi.</p>
</sec>
<sec id="sec2dot8-ijms-17-01063"><title>2.8. Cell Organization Related Genes</title>
<p>Many cell organization related genes were also found to be regulated by HLB infection and most of them were downregulated at 13 wpi but upregulated at 26 wpi (<xref ref-type="app" rid="app1-ijms-17-01063">Table S3</xref>
). Notably, two <italic>phloem protein</italic>
genes (<italic>PP</italic>
), <italic>PP2-B2</italic>
(ciclev10005659m) and <italic>PP2A-1</italic>
(ciclev10016359m), were upregulated at 13 wpi and another <italic>PP</italic>
gene, <italic>PP2-A12</italic>
, was upregulated at 26 wpi.</p>
</sec>
<sec id="sec2dot9-ijms-17-01063"><title>2.9. Quantitative Real Time PCR (qRT-PCR) Result</title>
<p>To validate the DGE data, quantitative Real Time PCR (qRT-PCR) was performed to investigate the transcriptional patterns of six representative genes as shown in <xref ref-type="fig" rid="ijms-17-01063-f005">Figure 5</xref>
. The upregulated expression patterns of the <italic>MYB</italic>
and <italic>HSP70</italic>
genes detected by qRT-PCR were in accordance with the DEG profile results. Similarly, the qRT-PCR detected downregulation in the expression of <italic>ERF</italic>
, <italic>KAR</italic>
, <italic>β-1,3-glucanase</italic>
was also in accordance with the DGE profile results that showed the three genes were downregulated more significantly at 13 wpi than at 26 wpi. <italic>Cyclophilin</italic>
was also found to be downregulated at 13 wpi by both qRT-PCR and DGE analysis, although it showed still a downregulation by qRT-PCR but an upregulation by DEG data at 26 wpi. Moreover, the temporal expression trends for all qRT-PCR verified genes were generally in agreement with those shown by DEG profiling data.</p>
</sec>
</sec>
<sec id="sec3-ijms-17-01063"><title>3. Discussion</title>
<p>Most of the previous reports on the early responses of citrus to <italic>C</italic>
Las infection used graft-transmitted citrus materials [<xref rid="B11-ijms-17-01063" ref-type="bibr">11</xref>
,<xref rid="B14-ijms-17-01063" ref-type="bibr">14</xref>
,<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
,<xref rid="B16-ijms-17-01063" ref-type="bibr">16</xref>
,<xref rid="B17-ijms-17-01063" ref-type="bibr">17</xref>
,<xref rid="B20-ijms-17-01063" ref-type="bibr">20</xref>
,<xref rid="B21-ijms-17-01063" ref-type="bibr">21</xref>
]. Obviously, graft-transmission has been largely responsible for the wide and rapid spread of the disease in many countries [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
]. However, the disease is naturally transmitted by ACP in open fields though it can be vectored by dodders in neglected orchards. Numerous reports have shown that inoculation by grafting with HLB-carrying budwoods required 50 days [<xref rid="B21-ijms-17-01063" ref-type="bibr">21</xref>
] to more than two months [<xref rid="B26-ijms-17-01063" ref-type="bibr">26</xref>
] for the bacteria to grow to a detectable level. But it is indicated that ACP was a more efficient vector, for HLB bacteria could be detected in less than seven days in leaves of jasmine oranges after exposing the trees to HLB-carrying ACPs [<xref rid="B26-ijms-17-01063" ref-type="bibr">26</xref>
]. In this study, we also found that psyllids were an efficient vector since HLB bacteria were detected within less than 3 wpi by conventional PCR.</p>
<p>Given the importance of leaves in photosynthesis and export of carbohydrates and in HLB symptom development, changes in gene expression in HLB infected citrus was first investigated in <italic>C</italic>
Las infected Valencia orange (<italic>Citrus sinensis</italic>
L. Osbeck) leaves in 2008 by Albrecht and Bowman [<xref rid="B14-ijms-17-01063" ref-type="bibr">14</xref>
]. Later, many studies were also performed by using <italic>C</italic>
Las infected leaves of sweet oranges (<italic>C. sinensis</italic>
), Cleopatra mandarins (<italic>C.</italic>
<italic>reticulata</italic>
), and rough lemon (<italic>C. jambhiri</italic>
) in various disease development stages [<xref rid="B8-ijms-17-01063" ref-type="bibr">8</xref>
,<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
,<xref rid="B16-ijms-17-01063" ref-type="bibr">16</xref>
,<xref rid="B17-ijms-17-01063" ref-type="bibr">17</xref>
]. In this study, we extended the research to ponkan, a very important mandarin cultivar that had dominated the citrus production in Guangdong province of China in the 1980s and was almost totally wiped out by HLB in late 1990s. With the use of DGE profiling we were able to find the dramatic differences between the transcriptomes of leaves from HLB infected and healthy ponkan trees at two representative time points, 13 and 26 wpi.</p>
<p>Previous studies reported that HLB-infection evoked defensive reactions in citrus for defense genes were general mostly upregulated [<xref rid="B11-ijms-17-01063" ref-type="bibr">11</xref>
,<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
,<xref rid="B21-ijms-17-01063" ref-type="bibr">21</xref>
]. We also found that ACP-transmitted HLB infection induced an overwhelmingly defensive reaction in ponkan leaves at 26 wpi as shown by the upregulation in many genes involved in cell-wall modifications, protein synthesis, transport, DNA synthesis, secondary metabolism, and auxin involved hormone signaling pathways (<xref ref-type="table" rid="ijms-17-01063-t002">Table 2</xref>
). However, a different picture was shown as we examine our data obtained from 13 wpi, which clearly showed that a substantial number of ponkan defense genes responded to <italic>C</italic>
Las by downregulating their expression at this early stage. The significance of the finding is that ponkan’s defense waned at the early stage, possibly from a rapid build up in <italic>C</italic>
Las population in consideration of a more natural vector, ACP, was used in our study.</p>
<p>Carbohydrates account for a large part of the translocated materials in phloem, and sucrose was reported to be the predominant sugar in phloem sieve tubes [<xref rid="B28-ijms-17-01063" ref-type="bibr">28</xref>
]. In our study, <italic>SPS</italic>
gene (ciclev10018655m) and <italic>β-fructofuranosidase</italic>
/<italic>invertase</italic>
gene (ciclev10019134m) were the two sucrose and starch metabolism related genes that were upregulated at both 13 and 26 wpi. Invertase was reported to play a key role in the activation of stress responses and may function as an extracellular indicator for pathogen infection [<xref rid="B29-ijms-17-01063" ref-type="bibr">29</xref>
,<xref rid="B30-ijms-17-01063" ref-type="bibr">30</xref>
]. AGPase (ADP-glucose pyrophosphorylase) is the key enzyme catalyzing the rate-limiting step in starch biosynthesis [<xref rid="B31-ijms-17-01063" ref-type="bibr">31</xref>
], and the repression of <italic>AGPase</italic>
and the upregulation of starch degradation related genes at 26 wpi may be a feedback regulation from accumulated starches in leaves. Other sugar metabolism pathways were also found to be affected by HLB infection. Galactinol and raffinose can protect plants from oxidative damage [<xref rid="B32-ijms-17-01063" ref-type="bibr">32</xref>
]. Galactinol synthase is the first enzyme in raffinose synthesis and regulates the partitioning between sucrose and raffinose, and was hypothesized to function in reducing sucrose level in phloem of HLB infected leaves and in scavenging reactive oxygen species (ROS) [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
]. The significant upregulation of the two galactinol synthase genes suggested that the sucrose levels might be accumulated following HLB-infection, possibly from the above mentioned increase in invertase activity.</p>
<p><italic>C</italic>
Las infection has been suggested to result in blockage of translocation [<xref rid="B10-ijms-17-01063" ref-type="bibr">10</xref>
]. The blockage comes partly from deposition of callose (β-1,3 glucan), which has been repeatedly observed in the sieve pores [<xref rid="B7-ijms-17-01063" ref-type="bibr">7</xref>
,<xref rid="B33-ijms-17-01063" ref-type="bibr">33</xref>
]. Callose synthesis can be induced by diverse biotic and abiotic stresses [<xref rid="B33-ijms-17-01063" ref-type="bibr">33</xref>
]. It has also been shown that mutant plants in which phloem transport is inhibited accumulate excessive callose around plasmodesmata in their phloem cell walls [<xref rid="B34-ijms-17-01063" ref-type="bibr">34</xref>
]. In <italic>C</italic>
Las infected citrus leaves, excessive callose formation in the phloem plasmodesmata preceded starch accumulation [<xref rid="B33-ijms-17-01063" ref-type="bibr">33</xref>
]. The upregulation of glucan synthase genes at a late stage might be related to callose deposition in HLB infected ponkan leaves. In addition, accumulation of phloem specific proteins at the sieve plates is also generally considered to cause the blockage of translocation stream [<xref rid="B35-ijms-17-01063" ref-type="bibr">35</xref>
]. In this respect, we found two upregulated phloem protein genes (<italic>PP</italic>
), <italic>PP2-B2</italic>
and <italic>PP2A-1</italic>
at 13 wpi and another upregulated <italic>PP</italic>
gene, <italic>PP2-A12</italic>
, at 26 wpi, and similar findings were reported in other studies [<xref rid="B8-ijms-17-01063" ref-type="bibr">8</xref>
,<xref rid="B14-ijms-17-01063" ref-type="bibr">14</xref>
,<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
].</p>
<p>Cell walls constitute the first defense barrier, protecting plants from bacterial infection. Cell wall metabolism was identified to be one of the most dramatically altered pathways in HLB-infected citrus trees [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
,<xref rid="B8-ijms-17-01063" ref-type="bibr">8</xref>
,<xref rid="B13-ijms-17-01063" ref-type="bibr">13</xref>
,<xref rid="B14-ijms-17-01063" ref-type="bibr">14</xref>
,<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
,<xref rid="B16-ijms-17-01063" ref-type="bibr">16</xref>
,<xref rid="B17-ijms-17-01063" ref-type="bibr">17</xref>
,<xref rid="B18-ijms-17-01063" ref-type="bibr">18</xref>
,<xref rid="B19-ijms-17-01063" ref-type="bibr">19</xref>
,<xref rid="B20-ijms-17-01063" ref-type="bibr">20</xref>
,<xref rid="B21-ijms-17-01063" ref-type="bibr">21</xref>
,<xref rid="B22-ijms-17-01063" ref-type="bibr">22</xref>
]. In this study, the cell wall-related genes were mostly downregulated at 13 wpi. Among them are <italic>IRX</italic>
genes that are involved in xylan biosynthesis and were reported to function in building the xylan backbone in the secondary and primary cell walls [<xref rid="B36-ijms-17-01063" ref-type="bibr">36</xref>
,<xref rid="B37-ijms-17-01063" ref-type="bibr">37</xref>
]. At 13 wpi, a <italic>IRX 12</italic>
was downregulated by more than eight-fold. At 26 wpi, however, two <italic>IRX12</italic>
were upregulated about 10-fold. In addition, many other cell-wall related genes were induced at 26 wpi including two significantly induced laccase genes. It is proposed that laccases play a role in the formation of lignin by promoting the oxidative coupling of monolignols [<xref rid="B38-ijms-17-01063" ref-type="bibr">38</xref>
].</p>
<p>PR proteins play important roles in plant defense against pathogens. At 13 wpi, most PR protein genes were found to be downregulated. It was reported that suppression of host defenses was critical for pathogenesis [<xref rid="B39-ijms-17-01063" ref-type="bibr">39</xref>
], and hence it is conceivable that the suppression of <italic>PR</italic>
genes should favor <italic>C</italic>
Las infection. At 26 wpi, however, most of the <italic>PR</italic>
genes were upregulated, which might be an indication for the eventual activation of defense mechanisms that lead to processes such as callose deposition in and around phloem tissues [<xref rid="B40-ijms-17-01063" ref-type="bibr">40</xref>
].</p>
<p>Some transcription factors, such as WRKYs and MYBs, could bind to promoter elements of individual defense related genes and were closely related to plant defense [<xref rid="B8-ijms-17-01063" ref-type="bibr">8</xref>
]. MYB transcription factors play important roles in many processes including stress response [<xref rid="B41-ijms-17-01063" ref-type="bibr">41</xref>
]. At 13 wpi, a <italic>LHY</italic>
and an <italic>EPR1</italic>
were upregulated by more than four-fold. These two genes were reported to play critical roles in regulating circadian rhythm [<xref rid="B42-ijms-17-01063" ref-type="bibr">42</xref>
,<xref rid="B43-ijms-17-01063" ref-type="bibr">43</xref>
]. Altered expression of these genes can cause abnormal circadian rhythms which, in turn, would lead to the disorders of clock-regulated pathways, such as photosynthesis, transport of sugars, and starch metabolism [<xref rid="B17-ijms-17-01063" ref-type="bibr">17</xref>
,<xref rid="B44-ijms-17-01063" ref-type="bibr">44</xref>
]. Correspondingly, the repression in photosynthesis and carbohydrate metabolism has been observed in HLB infected ponkan at 13 wpi. At 26 wpi, however, the same <italic>LHY</italic>
gene (ciclev10018966m) was downregulated about two-fold, which may indicate an eventual failure in the regulation of these vital processes.</p>
<p>The expression of secondary metabolism related genes were mostly downregulated at 13 wpi but mostly upregulated at 26 wpi. However, one wax metabolism related gene <italic>WAX2/CER3</italic>
(ciclev10007738m) was upregulated more than two-fold while two <italic>cerberus1</italic>
(<italic>CER1</italic>
) were downregulated at 26 wpi. The <italic>Arabidopsiswax2</italic>
is involved in cuticle membrane and wax production [<xref rid="B45-ijms-17-01063" ref-type="bibr">45</xref>
,<xref rid="B46-ijms-17-01063" ref-type="bibr">46</xref>
]. <italic>CER1</italic>
expression was reported to be induced by osmotic stresses and regulated by abscisic acid [<xref rid="B47-ijms-17-01063" ref-type="bibr">47</xref>
]. However, <italic>CER1</italic>
over-expression could increase susceptibility to bacterial and fungal pathogens [<xref rid="B47-ijms-17-01063" ref-type="bibr">47</xref>
]. The downregulation of <italic>CER1</italic>
at 26 wpi might be important for increasing the tolerance of ponkan to <italic>C</italic>
Las infection.</p>
<p>Vitamin E deficient 2 (VTE2) is the first enzyme of tocopherol biosynthesis pathways and is involved in phloem sucrose loading [<xref rid="B48-ijms-17-01063" ref-type="bibr">48</xref>
]. The loss of VTE2 function-mutants leaded to a phenotype that resembles HLB symptom in citrus [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
]. <italic>VTE2</italic>
was downregulated in asymptomatic <italic>C</italic>
Lam-infected citrus leaves [<xref rid="B5-ijms-17-01063" ref-type="bibr">5</xref>
] as shown in our study at 13 wpi, but significantly upregulated at 26 wpi. The downregulation of <italic>VTE2</italic>
in the early stage (13 wpi) might contribute to HLB symptom development and the upregulation of it in the late stage (26 wpi) might indicate a need for restoring normal phloem translocation of nutrients.</p>
<p>Hormone biosynthesis and signaling were significantly regulated by HLB infection. 2OG-Fe(II) oxygenase is involved in biosynthesis of secondary metabolites including flavonoids and gibberellins. The basal expression of this gene was also reported to be much higher in HLB tolerant species US-897 [<xref rid="B15-ijms-17-01063" ref-type="bibr">15</xref>
]. The significant upregulation of <italic>2OG-Fe(II) oxygenase</italic>
at 13 wpi might play a role in resistance against HLB. Auxins play a key role in plant development and the auxin response pathway is connected to the SA, JA, and ethylene (ET) signaling network in various ways [<xref rid="B13-ijms-17-01063" ref-type="bibr">13</xref>
]. Auxin metabolism was found to be significantly modulated by HLB infection at 26 wpi. At the same time, most of the ethylene and JA related DEGs were found to be upregulated. <italic>GGPS1</italic>
, catalyzing the formation of geranylgeranyl pyrophosphate, was reported to be induced by JA- or methyl salicylate (MeSA)- treatment [<xref rid="B49-ijms-17-01063" ref-type="bibr">49</xref>
], and a transcript of <italic>GGPS1</italic>
was upregulated about 10-fold at 26 wpi. Put together, a complex hormone regulation should be involved in the response of ponkan to HLB infection.</p>
<p>RLKs, calcium modulating proteins and G-proteins were involved in signaling and regulation of plant defense and defense response, and the expression of these genes was not only significantly regulated in HLB infected ponkan leaves as shown in our study but was also identified in HLB infected fruits and roots [<xref rid="B1-ijms-17-01063" ref-type="bibr">1</xref>
,<xref rid="B21-ijms-17-01063" ref-type="bibr">21</xref>
].</p>
<p>The ubiquitin/proteasome system (UPS) has been involved in the signaling transduction of stimuli and in the perception and signaling of plant hormones [<xref rid="B50-ijms-17-01063" ref-type="bibr">50</xref>
]. Several <italic>HSP70</italic>
genes, which are involved in signal transduction leading to plant defense responses [<xref rid="B51-ijms-17-01063" ref-type="bibr">51</xref>
], were found to be upregulated at both 13 and 26 wpi. We also found that the expression of many other heat shock proteins was suppressed at 13 wpi, and a reduction in HSP proteins was thought to be responsible for increased protein misfolding [<xref rid="B19-ijms-17-01063" ref-type="bibr">19</xref>
].</p>
<sec><title>Transport Related Genes Regulated by HLB Infection</title>
<p>Four <italic>PIPs</italic>
genes were found to be upregulated at 13 wpi. PIPs are aquaporins and are responsible for passive transmembrane transport of water and other small molecules [<xref rid="B52-ijms-17-01063" ref-type="bibr">52</xref>
]. Yeast cells expressing <italic>Vitis</italic>
aquaporins were reported to be osmosensitive [<xref rid="B53-ijms-17-01063" ref-type="bibr">53</xref>
]. Swelling in the middle lamella was observed in the presymptomatic leaves of <italic>C</italic>
Las infected trees [<xref rid="B7-ijms-17-01063" ref-type="bibr">7</xref>
]. The upregulation of these genes might function in promoting water and mineral transport in HLB infected ponkan leaves at the early stage of infection. The upregulation of transport related DEGs at 26 wpi might be driven by nutrient deficiency, which contrasts their counterparts that showed repression in <italic>C</italic>
Las infected sweet orange shoots [<xref rid="B20-ijms-17-01063" ref-type="bibr">20</xref>
].</p>
<p>In conclusion, our result showed that ACP-transmitted <italic>C</italic>
Las infection weakened quickly the defense of ponkan as shown by reduced expression of many defense genes at early stage (13 wpi), and a seeming reactivation of defense at symptomatic stage of 26 wpi since DEG data obtained at 26 wpi showed an upregulation in most genes involved in carbohydrate metabolism, plant defense, hormone signaling, secondary metabolism, transcription regulation, and other pathways.</p>
</sec>
</sec>
<sec id="sec4-ijms-17-01063"><title>4. Materials and Methods</title>
<sec id="sec4dot1-ijms-17-01063"><title>4.1. Asian Citrus Psyllids Collection and Feeding</title>
<p>ACP adults were collected from new flushes of jasmine orange (<italic>Murraya</italic>
<italic>paniculata</italic>
) in spring of 2009 and used to establish a laboratory colony. The colony was maintained on disease-free jasmine orange seedlings in net cages. Eggs were transferred to disease-free jasmine orange seedlings to get disease-free ACPs, and the fourth instar nymphs were transferred to <italic>C</italic>
Las-positive Hongjiangcheng (<italic>Citrus sinensis</italic>
Osbeck cv. “Hongjiangcheng”) trees for 20 days to obtain <italic>C</italic>
Las-carrying ACP adults. All the experiments were conducted under screen houses.</p>
</sec>
<sec id="sec4dot2-ijms-17-01063"><title>4.2. HLB Inoculation and Detection</title>
<p>Ponkan seeds were sown in sterilized soil in February 2008, and were used for the experiment at 31 August 2009. Five ponkan seedlings were exposed to 40 <italic>C</italic>
Las-carrying ACP adults for 3 days. For controls, 5 ponkan seedlings were exposed to 40 disease-free ACP adults. PCR was performed every week to detect the presence of <italic>C</italic>
Las in leaves of the samples using A2/J5 primers [<xref rid="B54-ijms-17-01063" ref-type="bibr">54</xref>
].</p>
</sec>
<sec id="sec4dot3-ijms-17-01063"><title>4.3. RNA Preparation and Digital Gene Expression Profiling</title>
<p>Fully expanded leaves were sampled from three HLB positive trees, respectively, at 13 wpi when chlorosis was barely discernible at the lower leaf areas, and at 26 wpi when typical mottling chlorosis symptoms developed. Leaf samples were also collected from the control trees. Total RNA was extracted using Trizol reagent according to manufacturer's instruction and treated with RNase-free DNase I (TaKaRa, Dalian, China) to remove contaminated DNA. The quality and quantity of the purified RNA were determined by measuring the absorbance at 260/280 nm (A260/A280) using NanoDrop 2000c UV-Vis Spectrophotometer (Thermo Scientific, Wilmington, DE, USA). RNA integrity was as assessed on 1% agarose gels. RNA samples were then pooled by treatment by taking an equal amount of RNA aliquot from each of the three RNA samples of the same treatment, and the four pooled samples were sent to the Beijing Genomics Institute (BGI; Shenzhen, China) for digital gene expression profiling. Sequencing was carried on Illumina HiSeq™ 2000 platform by using sequencing by synthesis (SBS) method. Millions of 35 nt (CATG + 17 nt gene sequence + 14 nt 3′ adaptor sequence) long raw sequences were generated.</p>
</sec>
<sec id="sec4dot4-ijms-17-01063"><title>4.4. Differential Gene Expression Analysis</title>
<p>Clean reads were obtained from raw sequencing data by removing the reads containing adapter or ploy-N and those of low quality. These reads were aligned to <italic>Citrus clementina</italic>
gene sequences (available at: <uri xlink:type="simple" xlink:href="http://www.phytozome.org">http://www.phytozome.org</uri>
.) using SOAP2 [<xref rid="B55-ijms-17-01063" ref-type="bibr">55</xref>
] in 2011. Number of distinct gene sequences was calculated using total numbers of clean tags that could be perfectly mapped. TPM (Transcripts Per Million) was used for relative assessment of gene expression levels. DEGs were identified by the DESeq R package [<xref rid="B56-ijms-17-01063" ref-type="bibr">56</xref>
]. Corrected <italic>p</italic>
-value < 0.005, FDR ≤ 0.001 and the absolute value of log<sub>2</sub>
(ratio) ≥ 1.5 were set as the thresholds for identifying significantly differential expressed genes. Two pairwise comparisons were made between samples of the HLB infected and the control samples collected at 13 wpi and at 26 wpi.</p>
<p>All the DEGs with gene IDs of the old version (Cclementina_165) were once again aligned with the new version of Clementine genome (Cclementina_182) and used for MapMan analysis in 2014. Pathway analysis was performed using PageMan embedded in the free-downloadable software MapMan [<xref rid="B57-ijms-17-01063" ref-type="bibr">57</xref>
]. A Wilcoxon test was applied and a statistics-based overview of changed pathways from global gene expression alteration was provided. The MapMan program was used to map the DEGs into specific pathways.</p>
<p>The raw data have been submitted to NCBI (BioProject ID: PRJNA318724).</p>
</sec>
<sec id="sec4dot5-ijms-17-01063"><title>4.5. Quantitative Real Time PCR (qRT-PCR) Analysis</title>
<p>To validate results obtained by digital gene expression profiles, aliquots of the same RNA samples were subjected to qRT-PCR analysis. Six representative genes including MYB transcription factor (MYB, ciclev10012263m), heat shock protein 70 (HSP70, ciclev10030928m), ERF transcription factor (ERF, ciclev10021285m), Ketol-acid reductoisomerase (KAR, ciclev10014720m), β-1,3-glucanase (B1,3G, ciclev10008176m) and cyclophilin (ciclev10029386m) were analyzed. cDNA was reverse-transcribed from the RNA samples using All-in-One™ qPCR Mix (GeneCopoeia) PrimeScript RT reagent kit (TaKaRa, Dalian, China). Primers specific to the 6 genes were designed with the Primer3 [<xref rid="B58-ijms-17-01063" ref-type="bibr">58</xref>
] and synthesized by BGI. Primers of internal reference gene β-actin were designed according to Cheng et al. [<xref rid="B59-ijms-17-01063" ref-type="bibr">59</xref>
]. All the primer sequences were listed in <xref ref-type="app" rid="app1-ijms-17-01063">Table S4</xref>
. The RT-qPCR was carried out on the thermocyclerCFX96 (Bio-Rad, Hercules, CA, USA) in a final volume of 20 µL containing 2 µL of cDNA, 10 µL 2× All-in-One™ (Genecopoeia, Rockville, MD, USA), 1 µL each of the forward and the reverse primers (10 µM), and 6 µL of sterile water. The thermocycler was programmed as: 95 °C for 10 min followed by 40 cycles of 95 °C for 5 s, 60 °C for 10 s and 72 °C for 15 s. The expression was calculated by 2<sup>−ΔΔ<italic>C</italic>
t</sup>
method [<xref rid="B60-ijms-17-01063" ref-type="bibr">60</xref>
] and normalized with the results of β-actin gene [<xref rid="B59-ijms-17-01063" ref-type="bibr">59</xref>
]. The amplification efficiency and the sizes of the amplicons were listed in <xref ref-type="app" rid="app1-ijms-17-01063">Table S4</xref>
. The curves of the first derivatives of the original qRT-PCR amplicons were single peaks (data not shown), indicating the quality of the PCR was acceptable. The results were shown as mean ± standard deviation from triplicate experiments. The significance of gene expression difference was calculated using <italic>t</italic>
-test based on the Δ<italic>C</italic>
<sub>t</sub>
values [<xref rid="B61-ijms-17-01063" ref-type="bibr">61</xref>
], which was carried out by SPSS version 19 (IBM, Chicago, IL, USA).</p>
</sec>
</sec>
<sec id="sec5-ijms-17-01063"><title>5. Conclusions</title>
<p>Global gene expression profiling reveled that there were more down-regulated than up-regulated genes in leaves of ponkan (<italic>C. reticulata</italic>
) mandarin trees following psyllid-transmission of HLB at 13 wpi, and classification of the affected genes indicated that the defense of the trees at the early stage of infection was compromised. However, the defensive responses were apparently activated at later stage of 26 wpi as was shown by changes in the expression of defense-related genes. The results indicated that a delayed defensive response to the fast growing bacteria might be responsible for the failure of Ponkan in fighting against HLB infection.</p>
</sec>
</body>
<back><ack><title>Acknowledgments</title>
<p>This work was supported by the International Science & Technology Cooperation Program of China (project No. 2012DFA30610), and by Guangdong provincial Science and technology Program (project No. 2014B020202009, 2014B070706018, 2014B020203003 and 2016B020201006).</p>
</ack>
<app-group><app id="app1-ijms-17-01063"><title>Supplementary Materials</title>
<p>Supplementary materials can be found at <uri xlink:type="simple" xlink:href="http://www.mdpi.com/1422-0067/17/7/1063/s1">http://www.mdpi.com/1422-0067/17/7/1063/s1</uri>
. Figure S1: PCR detection for Citrus Huanglongbing (HLB) bacteria in leaves at 3 wpi, Table S1: Mapman analysis result of the 3056 DEGs identified at 13 wpi, Table S2: Mapman analysis result of the 2522 DEGs identified at 26 wpi, Table S3: Mapman analysis result of the 585 DEGs identified at both 13 and 26 wpi, Table S4: Primers used for Real Time PCR analysis.</p>
<supplementary-material content-type="local-data" id="ijms-17-01063-s001"><media xlink:href="ijms-17-01063-s001.zip"><caption><p>Click here for additional data file.</p>
</caption>
</media>
</supplementary-material>
</app>
</app-group>
<notes><title>Author Contributions</title>
<p>Yun Zhong and Chunzhen Cheng conceived and designed the experiments, wrote the paper; Chunzhen Cheng, Nonghui Jiang, Yongyan Zhang, Yongyan Zhang and Minlun Hu performed the experiments; Chunzhen Cheng, Minlun Hu, and Bo Jiang analyzed the data; Bo Jiang and Nonghui Jiang contributed reagents/materials/analysis tools; Guangyan Zhong guide the experiments and modify the paper.</p>
</notes>
<notes><title>Conflicts of Interest</title>
<p>The authors declare no conflict of interest.</p>
</notes>
<glossary><title>Abbreviations</title>
<array><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">HLB</td>
<td align="left" valign="top" rowspan="1" colspan="1">Citrus Huanglongbing</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">WPI</td>
<td align="left" valign="top" rowspan="1" colspan="1">weeks post inoculation</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">DGE</td>
<td align="left" valign="top" rowspan="1" colspan="1">digital gene expression</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">ACP</td>
<td align="left" valign="top" rowspan="1" colspan="1">Asian citrus psyllids</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">DEG</td>
<td align="left" valign="top" rowspan="1" colspan="1">Differentially expressed gene</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>C</italic>
Las</td>
<td align="left" valign="top" rowspan="1" colspan="1"><italic>Candidatus</italic>
L. asiaticus</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>C</italic>
lam</td>
<td align="left" valign="top" rowspan="1" colspan="1"><italic>Candidatus</italic>
L. americanus</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>C</italic>
Laf</td>
<td align="left" valign="top" rowspan="1" colspan="1"><italic>Candidatus</italic>
L. africanus</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">SPS</td>
<td align="left" valign="top" rowspan="1" colspan="1">sucrose-phosphate synthase</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">SPP1</td>
<td align="left" valign="top" rowspan="1" colspan="1">sucrose-phosphatase 1</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">LHY</td>
<td align="left" valign="top" rowspan="1" colspan="1">late elongated hypocotyls</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">EPR1</td>
<td align="left" valign="top" rowspan="1" colspan="1">early-phytochrome responsive 1</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">GGPS1</td>
<td align="left" valign="top" rowspan="1" colspan="1">geranylgeranyl pyrophosphate synthase 1</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">HPT1</td>
<td align="left" valign="top" rowspan="1" colspan="1">homogentisate phytyl transferase 1</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">IRX12</td>
<td align="left" valign="top" rowspan="1" colspan="1">irregular xylem 12</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">LAC</td>
<td align="left" valign="top" rowspan="1" colspan="1">laccase</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">RLK</td>
<td align="left" valign="top" rowspan="1" colspan="1">receptor like kinases</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">HSP</td>
<td align="left" valign="top" rowspan="1" colspan="1">heat shock protein</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">PIP</td>
<td align="left" valign="top" rowspan="1" colspan="1">plasma membrane intrinsic protein</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">PP</td>
<td align="left" valign="top" rowspan="1" colspan="1">phloem protein</td>
</tr>
<tr><td align="left" valign="top" rowspan="1" colspan="1">UPS</td>
<td align="left" valign="top" rowspan="1" colspan="1">ubiquitin/proteasome system</td>
</tr>
</tbody>
</array>
</glossary>
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<floats-group><fig id="ijms-17-01063-f001" position="float"><label>Figure 1</label>
<caption><p>Differential regulation of genes in leaves at 13 and 26 weeks post inoculation (wpi). Figures in the two parentheses indicate total numbers of differentially expressed genes (DEGs) identified in leaves 13 and 26 wpi, respectively. Figures before virgules indicate numbers of upregulated DEGs, and those after virgules indicate the downregulated.</p>
</caption>
<graphic xlink:href="ijms-17-01063-g001"></graphic>
</fig>
<fig id="ijms-17-01063-f002" position="float"><label>Figure 2</label>
<caption><p>Overview of the DEGs involved in metabolisms at 13 (<bold>A</bold>
) and 26 wpi (<bold>B</bold>
) respectively in ponkan leaves infected with Asian citrus psyllid (ACP)-vectored <italic>C</italic>
Las bacteria. The red show the genes that were significantly upregulated while the green show the significantly downregulated. CHO: Carbohydrate; TCA: Tricarboxylic acid cycle; OPP: Oxidative Pentose Phosphate; * Raffinose family metabolism; Grey dots: genes without significant expression difference, arrows were used to indicate the direction of the pathways.</p>
</caption>
<graphic xlink:href="ijms-17-01063-g002"></graphic>
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<fig id="ijms-17-01063-f003" position="float"><label>Figure 3</label>
<caption><p>Stress related DEGs regulated by <italic>C</italic>
Las infection at 13 wpi (<bold>A</bold>
) and 26 wpi (<bold>B</bold>
) respectively in ponkan leaves. Genes significantly upregulated by <italic>C</italic>
Las infection are displayed in red, and those downregulated are shown in green. HSPs: heat-shock proteins; bZIP: basic leucin zipper; ERF: Ethylene response factor; MAPK: mitogen-activated protein kinase; MYB: MYB family transcription factor; DOF: DNA binding with one finger. ABA: abscisic acid; SA: salicylic acid; JA: jasmonic acid; R gene: resistance gene; Misc.: miscellaneous, PR-protein: pathogenesis-related protein, WRKY: WRKY transcription factors, DOF: DNA-binding with one finger.</p>
</caption>
<graphic xlink:href="ijms-17-01063-g003"></graphic>
</fig>
<fig id="ijms-17-01063-f004" position="float"><label>Figure 4</label>
<caption><p>MapMan views of transport related genes that were differentially regulated after <italic>C</italic>
Las infection at 13 (<bold>A</bold>
) and 26 wpi (<bold>B</bold>
). Genes significantly upregulated by <italic>C</italic>
Las are displayed in red, and the downregulated are shown in green. * <italic>PIP</italic>
(plasma membrane intrinsic protein) genes; <italic>SIP</italic>
: small and basic intrinsic protein genes; <italic>NIP</italic>
: Nod26-like intrinsic protein genes; <italic>TIP</italic>
: tonoplast intrinsic protein genes; grid framed with ellipse represents chloroplast.</p>
</caption>
<graphic xlink:href="ijms-17-01063-g004"></graphic>
</fig>
<fig id="ijms-17-01063-f005" position="float"><label>Figure 5</label>
<caption><p>Comparison of the expression levels in ponkan leaves infected with <italic>C</italic>
Las relative to their controls of six of the representative genes obtained by real-time PCR (A,C) and by digital gene expression (DGE) profiles (B,D). A,B: at 13 wpi; C,D: at 26 wpi. * and ** indicate significant changes at <italic>p</italic>
< 0.05 and <italic>p</italic>
< 0.01, respectively. <italic>MYB</italic>
, MYB family transcription factor; HSP, heat-shock proteins; <italic>KAR</italic>
, ketol-acid reductoisomerase; <italic>BG</italic>
, β-1,3-glucanase; <italic>ERF</italic>
, Ethylene response factor.</p>
</caption>
<graphic xlink:href="ijms-17-01063-g005"></graphic>
</fig>
<table-wrap id="ijms-17-01063-t001" position="float"><object-id pub-id-type="pii">ijms-17-01063-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Statistical results of digital gene expression profiles. M1 and M2: control ponkan leaves sampled at 13 and 26 weeks post inoculation (wpi), respectively; H1 and H2: Citrus Huanglongbing infected ponkan leaves sampled at 13 and 26 wpi, respectively.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Summary Detail</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">M1</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">M2</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">H1</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">H2</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Number of total raw tags</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,587,092</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,696,000</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,704,176</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,587,500</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Number of distinct tags</td>
<td align="center" valign="middle" rowspan="1" colspan="1">200,301</td>
<td align="center" valign="middle" rowspan="1" colspan="1">207,328</td>
<td align="center" valign="middle" rowspan="1" colspan="1">191,280</td>
<td align="center" valign="middle" rowspan="1" colspan="1">230,525</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Number of total clean tags</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,479,412</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,558,497</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,602,015</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3,449,820</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Number of distinct tags</td>
<td align="center" valign="middle" rowspan="1" colspan="1">92,796</td>
<td align="center" valign="middle" rowspan="1" colspan="1">89,297</td>
<td align="center" valign="middle" rowspan="1" colspan="1">89,324</td>
<td align="center" valign="middle" rowspan="1" colspan="1">110,577</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Total clean tags mapped to Gene</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2,715,908</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2,778,658</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2,506,722</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2,668,438</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Percentage of clean tags mapped to Gene</td>
<td align="center" valign="middle" rowspan="1" colspan="1">78.06%</td>
<td align="center" valign="middle" rowspan="1" colspan="1">78.09%</td>
<td align="center" valign="middle" rowspan="1" colspan="1">69.59%</td>
<td align="center" valign="middle" rowspan="1" colspan="1">77.35%</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Number of distinct tags mapped to Gene</td>
<td align="center" valign="middle" rowspan="1" colspan="1">55,259</td>
<td align="center" valign="middle" rowspan="1" colspan="1">57,768</td>
<td align="center" valign="middle" rowspan="1" colspan="1">48,500</td>
<td align="center" valign="middle" rowspan="1" colspan="1">68,912</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Percentage of distinct tags mapped to Gene</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">59.55%</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">64.69%</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">54.30%</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">62.32%</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="ijms-17-01063-t002" position="float"><object-id pub-id-type="pii">ijms-17-01063-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>HLB-modulated pathways in ponkan leaves, showing the 12 pathways significantly changed following HLB infection at 26 wpi (<italic>p</italic>
-value ≤ 0.05).</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Bin ID</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Pathway Name</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">DEG Numbers</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>p</italic>
-Value</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">29.2.1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protein. synthesis. ribosomal protein</td>
<td align="center" valign="middle" rowspan="1" colspan="1">40</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2.81 × 10<sup>−</sup>
<sup>7</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">29.2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protein. synthesis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">55</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1.22 × 10<sup>−6</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">10</td>
<td align="center" valign="middle" rowspan="1" colspan="1">cell wall</td>
<td align="center" valign="middle" rowspan="1" colspan="1">71</td>
<td align="center" valign="middle" rowspan="1" colspan="1">6.35 × 10<sup>−5</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">29.2.1.2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protein. synthesis. ribosomal protein. eukaryotic</td>
<td align="center" valign="middle" rowspan="1" colspan="1">21</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3.46 × 10<sup>−4</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">34</td>
<td align="center" valign="middle" rowspan="1" colspan="1">transport</td>
<td align="center" valign="middle" rowspan="1" colspan="1">126</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5.49 × 10<sup>−3</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">28.1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DNA. synthesis/chromatin structure</td>
<td align="center" valign="middle" rowspan="1" colspan="1">26</td>
<td align="center" valign="middle" rowspan="1" colspan="1">7.96 × 10<sup>−3</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">29.2.1.2.1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protein. synthesis. ribosomal protein. Eukaryotic. 40S subunit</td>
<td align="center" valign="middle" rowspan="1" colspan="1">11</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2.24 × 10<sup>−2</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">28.1.3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">DNA. synthesis/chromatin structure. histone</td>
<td align="center" valign="middle" rowspan="1" colspan="1">7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2.65 × 10<sup>−2</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">10.2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">cell wall. cellulose synthesis</td>
<td align="center" valign="middle" rowspan="1" colspan="1">9</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3.18 × 10<sup>−2</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">16.1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">secondary metabolism. simple phenols</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4.46 × 10<sup>−2</sup>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">29.2.1.1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">protein. synthesis. ribosomal protein. prokaryotic</td>
<td align="center" valign="middle" rowspan="1" colspan="1">15</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4.46 × 10<sup>−2</sup>
</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">17.2</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">hormone metabolism. auxin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">4.62 × 10<sup>−2</sup>
</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Bin is the unit used in Mapman graphs denoting a pathway, organelles or gene, and each bin has been assigned a specific ID in Mapman; DEG, differentially expressed gene. Dots in Pathway Name are in accordance with the dots showing in the Bin ID column.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>
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