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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">cDNA-AFLP analysis reveals the adaptive responses of citrus to long-term boron-toxicity</title><author><name sortKey="Guo, Peng" sort="Guo, Peng" uniqKey="Guo P" first="Peng" last="Guo">Peng Guo</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Qi, Yi Ping" sort="Qi, Yi Ping" uniqKey="Qi Y" first="Yi-Ping" last="Qi">Yi-Ping Qi</name><affiliation><nlm:aff id="Aff3">Institute of Materia Medica, Fujian Academy of Medical Sciences, Fuzhou, 350001 China</nlm:aff></affiliation></author><author><name sortKey="Yang, Lin Tong" sort="Yang, Lin Tong" uniqKey="Yang L" first="Lin-Tong" last="Yang">Lin-Tong Yang</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Ye, Xin" sort="Ye, Xin" uniqKey="Ye X" first="Xin" last="Ye">Xin Ye</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Jiang, Huan Xin" sort="Jiang, Huan Xin" uniqKey="Jiang H" first="Huan-Xin" last="Jiang">Huan-Xin Jiang</name><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff4">College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Huang, Jing Hao" sort="Huang, Jing Hao" uniqKey="Huang J" first="Jing-Hao" last="Huang">Jing-Hao Huang</name><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff4">College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff5">Institute of Fruit Tree Science, Fujian Academy of Agricultural Sciences, Fuzhou, 350013 China</nlm:aff></affiliation></author><author><name sortKey="Chen, Li Song" sort="Chen, Li Song" uniqKey="Chen L" first="Li-Song" last="Chen">Li-Song Chen</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff6">Fujian Key Laboratory for Plant Molecular and Cell Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff7">The Higher Educational Key Laboratory of Fujian Province for Soil Ecosystem Health and Regulation, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25348611</idno><idno type="pmc">4219002</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4219002</idno><idno type="RBID">PMC:4219002</idno><idno type="doi">10.1186/s12870-014-0284-5</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000616</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">cDNA-AFLP analysis reveals the adaptive responses of citrus to long-term boron-toxicity</title><author><name sortKey="Guo, Peng" sort="Guo, Peng" uniqKey="Guo P" first="Peng" last="Guo">Peng Guo</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Qi, Yi Ping" sort="Qi, Yi Ping" uniqKey="Qi Y" first="Yi-Ping" last="Qi">Yi-Ping Qi</name><affiliation><nlm:aff id="Aff3">Institute of Materia Medica, Fujian Academy of Medical Sciences, Fuzhou, 350001 China</nlm:aff></affiliation></author><author><name sortKey="Yang, Lin Tong" sort="Yang, Lin Tong" uniqKey="Yang L" first="Lin-Tong" last="Yang">Lin-Tong Yang</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Ye, Xin" sort="Ye, Xin" uniqKey="Ye X" first="Xin" last="Ye">Xin Ye</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Jiang, Huan Xin" sort="Jiang, Huan Xin" uniqKey="Jiang H" first="Huan-Xin" last="Jiang">Huan-Xin Jiang</name><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff4">College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author><author><name sortKey="Huang, Jing Hao" sort="Huang, Jing Hao" uniqKey="Huang J" first="Jing-Hao" last="Huang">Jing-Hao Huang</name><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff4">College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff5">Institute of Fruit Tree Science, Fujian Academy of Agricultural Sciences, Fuzhou, 350013 China</nlm:aff></affiliation></author><author><name sortKey="Chen, Li Song" sort="Chen, Li Song" uniqKey="Chen L" first="Li-Song" last="Chen">Li-Song Chen</name><affiliation><nlm:aff id="Aff1">College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2">Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff6">Fujian Key Laboratory for Plant Molecular and Cell Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation><affiliation><nlm:aff id="Aff7">The Higher Educational Key Laboratory of Fujian Province for Soil Ecosystem Health and Regulation, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</nlm:aff></affiliation></author></analytic><series><title level="j">BMC Plant Biology</title><idno type="eISSN">1471-2229</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Boron (B)-toxicity is an important disorder in agricultural regions across the world. Seedlings of ‘Sour pummelo’ (<italic>Citrus grandis</italic>) and ‘Xuegan’ (<italic>Citrus sinensis</italic>) were fertigated every other day until drip with 10 μM (control) or 400 μM (B-toxic) H<sub>3</sub>BO<sub>3</sub> in a complete nutrient solution for 15 weeks. The aims of this study were to elucidate the adaptive mechanisms of citrus plants to B-toxicity and to identify B-tolerant genes.</p></sec><sec><title>Results</title><p>B-toxicity-induced changes in seedlings growth, leaf CO<sub>2</sub> assimilation, pigments, total soluble protein, malondialdehyde (MDA) and phosphorus were less pronounced in <italic>C. sinensis</italic> than in <italic>C. grandis</italic>. B concentration was higher in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones. Here we successfully used cDNA-AFLP to isolate 67 up-regulated and 65 down-regulated transcript-derived fragments (TDFs) from B-toxic <italic>C. grandis</italic> leaves, whilst only 31 up-regulated and 37 down-regulated TDFs from B-toxic <italic>C. sinensis</italic> ones, demonstrating that gene expression is less affected in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones. These differentially expressed TDFs were related to signal transduction, carbohydrate and energy metabolism, nucleic acid metabolism, protein and amino acid metabolism, lipid metabolism, cell wall and cytoskeleton modification, stress responses and cell transport. The higher B-tolerance of <italic>C. sinensis</italic> might be related to the findings that B-toxic <italic>C. sinensis</italic> leaves had higher expression levels of genes involved in photosynthesis, which might contribute to the higher photosyntheis and light utilization and less excess light energy, and in reactive oxygen species (ROS) scavenging compared to B-toxic <italic>C. grandis</italic> leaves, thus preventing them from photo-oxidative damage. In addition, B-toxicity-induced alteration in the expression levels of genes encoding inorganic pyrophosphatase 1, AT4G01850 and methionine synthase differed between the two species, which might play a role in the B-tolerance of <italic>C. sinensis</italic>.</p></sec><sec><title>Conclusions</title><p><italic>C. sinensis</italic> leaves could tolerate higher level of B than <italic>C. grandis</italic> ones, thus improving the B-tolerance of <italic>C. sinensis</italic> plants. Our findings reveal some novel mechanisms on the tolerance of plants to B-toxicity at the gene expression level.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12870-014-0284-5) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Nable, Ro" uniqKey="Nable R">RO Nable</name></author><author><name sortKey="Banuelos, Gs" uniqKey="Banuelos G">GS Banuelos</name></author><author><name sortKey="Paull, Jg" uniqKey="Paull J">JG Paull</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Papadakis, Ie" uniqKey="Papadakis I">IE Papadakis</name></author><author><name sortKey="Dimassi, Kn" uniqKey="Dimassi K">KN Dimassi</name></author><author><name sortKey="Therios, In" uniqKey="Therios I">IN Therios</name></author></analytic></biblStruct><biblStruct><analytic><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Plant Biol</journal-id><journal-id journal-id-type="iso-abbrev">BMC Plant Biol</journal-id><journal-title-group><journal-title>BMC Plant Biology</journal-title></journal-title-group><issn pub-type="epub">1471-2229</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25348611</article-id><article-id pub-id-type="pmc">4219002</article-id><article-id pub-id-type="publisher-id">284</article-id><article-id pub-id-type="doi">10.1186/s12870-014-0284-5</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>cDNA-AFLP analysis reveals the adaptive responses of citrus to long-term boron-toxicity</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Guo</surname><given-names>Peng</given-names></name><address><email>6253730@163.com</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Qi</surname><given-names>Yi-Ping</given-names></name><address><email>qiyiping2008@hotmail.com</email></address><xref ref-type="aff" rid="Aff3"></xref></contrib><contrib contrib-type="author"><name><surname>Yang</surname><given-names>Lin-Tong</given-names></name><address><email>Yang-talstoy@sina.com</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>Ye</surname><given-names>Xin</given-names></name><address><email>yexin1000@163.com</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Jiang</surname><given-names>Huan-Xin</given-names></name><address><email>jianghx@163.com</email></address><xref ref-type="aff" rid="Aff2"></xref><xref ref-type="aff" rid="Aff4"></xref></contrib><contrib contrib-type="author"><name><surname>Huang</surname><given-names>Jing-Hao</given-names></name><address><email>17629399@qq.com</email></address><xref ref-type="aff" rid="Aff2"></xref><xref ref-type="aff" rid="Aff4"></xref><xref ref-type="aff" rid="Aff5"></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Chen</surname><given-names>Li-Song</given-names></name><address><email>lisongchen2002@hotmail.com</email></address><xref ref-type="aff" rid="Aff1"></xref><xref ref-type="aff" rid="Aff2"></xref><xref ref-type="aff" rid="Aff6"></xref><xref ref-type="aff" rid="Aff7"></xref></contrib><aff id="Aff1"><label></label>College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</aff><aff id="Aff2"><label></label>Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</aff><aff id="Aff3"><label></label>Institute of Materia Medica, Fujian Academy of Medical Sciences, Fuzhou, 350001 China</aff><aff id="Aff4"><label></label>College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</aff><aff id="Aff5"><label></label>Institute of Fruit Tree Science, Fujian Academy of Agricultural Sciences, Fuzhou, 350013 China</aff><aff id="Aff6"><label></label>Fujian Key Laboratory for Plant Molecular and Cell Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</aff><aff id="Aff7"><label></label>The Higher Educational Key Laboratory of Fujian Province for Soil Ecosystem Health and Regulation, Fujian Agriculture and Forestry University, Fuzhou, 350002 China</aff></contrib-group><pub-date pub-type="epub"><day>28</day><month>10</month><year>2014</year></pub-date><pub-date pub-type="pmc-release"><day>28</day><month>10</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>14</volume><elocation-id>284</elocation-id><history><date date-type="received"><day>13</day><month>9</month><year>2014</year></date><date date-type="accepted"><day>14</day><month>10</month><year>2014</year></date></history><permissions><copyright-statement>© Guo et al.; licensee BioMed Central Ltd. 2014</copyright-statement><license license-type="open-access"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution 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>), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p>Boron (B)-toxicity is an important disorder in agricultural regions across the world. Seedlings of ‘Sour pummelo’ (<italic>Citrus grandis</italic>) and ‘Xuegan’ (<italic>Citrus sinensis</italic>) were fertigated every other day until drip with 10 μM (control) or 400 μM (B-toxic) H<sub>3</sub>BO<sub>3</sub> in a complete nutrient solution for 15 weeks. The aims of this study were to elucidate the adaptive mechanisms of citrus plants to B-toxicity and to identify B-tolerant genes.</p></sec><sec><title>Results</title><p>B-toxicity-induced changes in seedlings growth, leaf CO<sub>2</sub> assimilation, pigments, total soluble protein, malondialdehyde (MDA) and phosphorus were less pronounced in <italic>C. sinensis</italic> than in <italic>C. grandis</italic>. B concentration was higher in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones. Here we successfully used cDNA-AFLP to isolate 67 up-regulated and 65 down-regulated transcript-derived fragments (TDFs) from B-toxic <italic>C. grandis</italic> leaves, whilst only 31 up-regulated and 37 down-regulated TDFs from B-toxic <italic>C. sinensis</italic> ones, demonstrating that gene expression is less affected in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones. These differentially expressed TDFs were related to signal transduction, carbohydrate and energy metabolism, nucleic acid metabolism, protein and amino acid metabolism, lipid metabolism, cell wall and cytoskeleton modification, stress responses and cell transport. The higher B-tolerance of <italic>C. sinensis</italic> might be related to the findings that B-toxic <italic>C. sinensis</italic> leaves had higher expression levels of genes involved in photosynthesis, which might contribute to the higher photosyntheis and light utilization and less excess light energy, and in reactive oxygen species (ROS) scavenging compared to B-toxic <italic>C. grandis</italic> leaves, thus preventing them from photo-oxidative damage. In addition, B-toxicity-induced alteration in the expression levels of genes encoding inorganic pyrophosphatase 1, AT4G01850 and methionine synthase differed between the two species, which might play a role in the B-tolerance of <italic>C. sinensis</italic>.</p></sec><sec><title>Conclusions</title><p><italic>C. sinensis</italic> leaves could tolerate higher level of B than <italic>C. grandis</italic> ones, thus improving the B-tolerance of <italic>C. sinensis</italic> plants. Our findings reveal some novel mechanisms on the tolerance of plants to B-toxicity at the gene expression level.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12870-014-0284-5) contains supplementary material, which is available to authorized users.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Boron-tolerance</kwd><kwd>Boron-toxicity</kwd><kwd>cDNA-AFLP</kwd><kwd><italic>Citrus grandis</italic></kwd><kwd><italic>Citrus sinensis</italic></kwd><kwd>Photosynthesis</kwd></kwd-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2014</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1" sec-type="introduction"><title>Background</title><p>Althought boron (B) is a micronutrient element required for normal growth and development of higher plants, it is harmful to plants when present in excess. Whilst of lesser importance than B-deficiency (a widespread problem in many agricultural crops), B-toxicity is also an important problem in agricultural regions across the world, which citrus trees are cultivated [<xref ref-type="bibr" rid="CR1">1</xref>-<xref ref-type="bibr" rid="CR3">3</xref>]. Despite the importance of B-toxicity for crop productivity, the mechanisms by which plants respond to B-toxicity are poorly understood yet. Recently, increasing attention has been paid to plant B-toxicity as a result of the increased demand for desalinated water, in which the B level may be too high for healthy irrigation of crops [<xref ref-type="bibr" rid="CR4">4</xref>].</p><p>Alteration of gene expression levels is an inevitable process of plants responding to environmental stresses. Kasajima and Fujiwara first investigated high B-induced changes in gene expression in <italic>Arabidopsis thaliana</italic> roots and rosette leaves using microarray, and identified a number of high B-induced genes, including a heat shock protein and a number of the multi-drug and toxic compound extrusion (MATE) family transporters [<xref ref-type="bibr" rid="CR5">5</xref>]. Hassan et al. preformed suppression subtractive hybridization on root cDNA from bulked B-tolerant and -intolerant doubled haploid barley lines grown under moderate B-stress and identified 111 upregulated clones in the tolerant bulk under B-stress, nine of which were genetically mapped to B-tolerant quantitative trait loci. An antioxidative response mechanism was suggested to provide an advantage in tolerating high level of soil B [<xref ref-type="bibr" rid="CR6">6</xref>]. Recently, Aquea et al. found that B-toxicity upregulated the expression of genes related to ABA signaling, ABA response and cell wall modification, and downregulated the expression of genes involved in water transporters in <italic>Arabidopsis</italic> roots, concluding that root growth inhibition was caused by B-toxicity-induced water-stress [<xref ref-type="bibr" rid="CR7">7</xref>]. Most research, however, has focused on roots and herbaceous plants (i.e., barley, <italic>A. thaliana</italic>), very little is known about the differential expression of genes in response to B-toxicity in leaves and woody plants.</p><p>Citrus belongs to evergreen subtropical fruit trees. In China, B-toxicity often occurs in citrus orchards from high level of B in soils and/or irrigation water and from inappropriate application of B fertilizer especially under low-rainfall conditions [<xref ref-type="bibr" rid="CR8">8</xref>,<xref ref-type="bibr" rid="CR9">9</xref>]. During 1998–1999, Huang et al. investigated the nutrient status of soils and leaves from 200 ‘Guanximiyou’ pummelo (<italic>Citrus grandis</italic>) orchards located in Pinghe, Zhangzhou, China. Up to 61.5% and 17.0% of orchards were excess in leaf B and soil water-soluble B, respectively [<xref ref-type="bibr" rid="CR10">10</xref>]. Previous studies showed that B-toxicity disturbed citrus plant growth and metabolism in multiple way, including interference of nutrient uptake [<xref ref-type="bibr" rid="CR2">2</xref>], ultrastructural damage of roots and leaves [<xref ref-type="bibr" rid="CR11">11</xref>-<xref ref-type="bibr" rid="CR13">13</xref>], inhibition of CO<sub>2</sub> assimilation, photosynthetic enzymes and photosynthetic electron transport, decrease of chlorophyll (Chl), carotenoid (Car) and total soluble protein levels, affecting leaf carbohydrate metabolism and antioxidant system [<xref ref-type="bibr" rid="CR9">9</xref>,<xref ref-type="bibr" rid="CR14">14</xref>]. However, our understanding of the molecular mechanisms underlying these processes in citrus is very limited. To our best knowledge, no high B-toxicity-induced changes in gene expression profiles have been reported in citrus plants to date. Here we investigated the effects of B-toxicity on growth, leaf CO<sub>2</sub> assimilation, leaf concentrations of malondialdehyde (MDA), pigments and total soluble protein, root and leaf concentration of B, leaf concentration of phosphorus (P), and leaf gene expression profiles using cDNA-amplified fragment length polymorphism (cDNA-AFLP) in <italic>Citrus grandis</italic> and <italic>Citrus sinensis</italic> seedlings differing in B-tolerance [<xref ref-type="bibr" rid="CR13">13</xref>]. The aims of this study were to elucidate the adaptive mechanisms of citrus plants to B-toxicity and to identify B-tolerant genes.</p></sec><sec id="Sec2" sec-type="results"><title>Results</title><sec id="Sec3"><title>Effects of B-toxicity on seedlings growth, B concentration in roots and leaves, and P concentration in leaves</title><p>Because B is phloem immobile in citrus plants, B-toxic symptoms first developed in old leaves. The typical visible symptom produced in B-toxic leaves was leaf burn (chlorotic and/or necrotic), which only occurred in <italic>C. grandis</italic> plants. In the later stages, B-toxic leaves shed premature. By contrast, almost no visible symptoms occurred in <italic>C. sinensis</italic> plants except for very few plants (Additional file <xref rid="MOESM1" ref-type="media">1</xref>).</p><p>B-toxicity-induced decreases in root, shoot and whole plant dry weights (DWs) were more pronounced in <italic>C. grandis</italic> than in <italic>C. sinensis</italic> seedlings (Figure <xref rid="Fig1" ref-type="fig">1</xref>A-C). Root DW decreased to a larger extent than shoot DW in response to B-toxicity, and resulted in a decrease in root DW/shoot DW ratio of both <italic>C. grandis</italic> and <italic>C. sinensis</italic> seedlings (Figure <xref rid="Fig1" ref-type="fig">1</xref>A-B and D).<fig id="Fig1"><label>Figure 1</label><caption><p><bold>Effects of B</bold>-<bold>toxicity on growth of</bold><bold><italic>Citrus sinensis</italic></bold><bold>and</bold><bold><italic>C. grandis</italic></bold><bold>seedlings.</bold> Bars represent means ± SE (<italic>n</italic> =10). <bold>(A</bold><bold>-C)</bold> Root, shoot and root + shoot DWs. <bold>(D)</bold> Ratio of root DW to shoot DW. Bars represent means ± SE (<italic>n</italic> =10). Different letters above the bars indicate a significant difference at <italic>P</italic> <0.05.</p></caption><graphic xlink:href="12870_2014_284_Fig1_HTML" id="MO1"></graphic></fig></p><p>B-toxicity increased B concentration in roots and leaves, especially in leaves and decreased P concentration in <italic>C. grandis</italic> leaves. No significant differences were found in root and leaf B concentration and leaf P concentration between the two species at each given B treatment except that B concentration was higher in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic C. <italic>grandis</italic> ones (Figure <xref rid="Fig2" ref-type="fig">2</xref>).<fig id="Fig2"><label>Figure 2</label><caption><p><bold>Effects of B</bold>-<bold>toxicity on root and leaf B and leaf P.</bold><bold>(A-</bold><bold>B)</bold> Root and leaf B concentration. <bold>(C)</bold> Leaf P concentration. Bars represent means ± SE (<italic>n</italic> =4 or 5). Different letters above the bars indicate a significant difference at <italic>P</italic> <0.05.</p></caption><graphic xlink:href="12870_2014_284_Fig2_HTML" id="MO2"></graphic></fig></p></sec><sec id="Sec4"><title>Effects of B-toxicity on leaf gas exchange, pigments, total soluble protein and MDA</title><p>B-toxicity-induced decreases in both CO<sub>2</sub> assimilation and stomatal conductance were higher in <italic>C. grandis</italic> than in <italic>C. sinensis</italic> leaves. Intercellular CO<sub>2</sub> concentration increased in <italic>C. grandis</italic> leaves, but did not significantly change in <italic>C. sinensis</italic> leaves in response to B-toxicity. CO<sub>2</sub> assimilation and stomatal conductance in control leaves did not differ between the two species, but were higher in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones. Intercellular CO<sub>2</sub> concentration in control leaves was higher in <italic>C. sinensis</italic> than in <italic>C. grandis</italic>, but the reverse was the case in B-toxic leaves (Figure <xref rid="Fig3" ref-type="fig">3</xref>A-C).<fig id="Fig3"><label>Figure 3</label><caption><p><bold>Effects of B</bold>-<bold>toxicity on leaf gas exchange</bold>, <bold>total soluble protein</bold>, <bold>pigments and MDA.</bold><bold>(A-</bold><bold>C)</bold> CO<sub>2</sub> assimilation, stomatal conductance and intercellular CO<sub>2</sub> concentration. <bold>(D)</bold> Total soluble protein concentration. <bold>(E)</bold> Chl a + b concentration. <bold>(F)</bold> Chl a/b ratio. <bold>(G)</bold> Car concentration. <bold>(H)</bold> MDA concentration. Bars represent means ± SE (<italic>n</italic> =4 or 5). Different letters above the bars indicate a significant difference at <italic>P</italic> <0.05.</p></caption><graphic xlink:href="12870_2014_284_Fig3_HTML" id="MO3"></graphic></fig></p><p>B-toxicity decreased concentrations of Chl a + b and Car and ratio of Chl a/b in <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves. In control leaves, all the three parameters did not differ between the two species, but Chl a + b and Car concentrations were higher in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones (Figure <xref rid="Fig3" ref-type="fig">3</xref>E-G).</p><p>Leaf concentrations of total soluble protein and MDA were decreased and increased by B-toxicity in <italic>C. grandis</italic> leaves, respectively, but were not significantly affected in <italic>C. sinensis</italic> ones (Figure <xref rid="Fig3" ref-type="fig">3</xref>D and H).</p></sec><sec id="Sec5"><title>B-toxicity-induced differentially expressed genes revealed by cDNA-AFLP</title><p>Here we used a total of 256 selective primer combinations to isolate the differentially expressed transcript-derived fragments (TDFs) from B-toxic leaves of two citrus species differing in B-tolerance. A representative picture of a silver-stained cDNA-AFLP gel showing B-toxicity-induced genes in <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves was presented in Additional file <xref rid="MOESM2" ref-type="media">2</xref>. As shown in Table <xref rid="Tab1" ref-type="table">1</xref>, a total of 6050 clear and unambiguous TDFs were detected from the B-toxic leaves, with an average of 25.7 (15–40) TDFs for each primer combination. Among these TDFs, 932 TDFs only presented in <italic>C. grandi</italic>s, 631 TDFs only presented in <italic>C. sinensis</italic>, and 4587 TDFs presented in the two species.<table-wrap id="Tab1"><label>Table 1</label><caption><p><bold>Summary of transcript</bold>-<bold>derived fragments</bold> (<bold>TDFs</bold>) <bold>from control and boron</bold> (<bold>B</bold>)-<bold>toxic leaves of</bold><bold><italic>Citrus grandis</italic></bold><bold>and</bold><bold><italic>Citrus sinensis</italic></bold></p></caption><table frame="hsides" rules="groups"><thead><tr valign="top"><th rowspan="2"></th><th colspan="4"><bold>Number of TDFs</bold></th></tr><tr valign="top"><th><bold>Only present in</bold><bold><italic>C. grandis</italic></bold></th><th><bold>Only present in</bold><bold><italic>C. sinensis</italic></bold></th><th><bold>Present in both species</bold></th><th><bold>Total</bold></th></tr></thead><tbody><tr valign="top"><td>Total TDFs detected from gels</td><td>932</td><td>631</td><td>4487</td><td>6050</td></tr><tr valign="top"><td>Total differentially expressed TDFs recovered from gels</td><td>164</td><td>50</td><td>54</td><td>268</td></tr><tr valign="top"><td>TDFs produced useable sequence data</td><td>139</td><td>46</td><td>44</td><td>229</td></tr><tr valign="top"><td>TDFs encoding known or putative proteins</td><td>97</td><td>40</td><td>23</td><td>160</td></tr><tr valign="top"><td>TDFs encoding predicted, uncharacterized, hypothetical or unnamed proteins</td><td>9</td><td>2</td><td>3</td><td>14</td></tr><tr valign="top"><td>TDFs without database matches</td><td>33</td><td>4</td><td>18</td><td>55</td></tr></tbody></table></table-wrap></p><p>A total of 218 and 104 differentially expressed and reproducible TDFs were successfully obtained from B-toxic <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves, respectively. All these TDFs were re-amplified, cloned and sequenced. For <italic>C. grandis</italic>, 183 of fragments yielded usable sequence data. Aligment analysis showed 132 TDFs were homologous to genes encoding known, putative predicted, uncharacterized, hypothetical or unnamed proteins, and the remaining 51 TDFs showed no significant matches (Tables <xref rid="Tab1" ref-type="table">1</xref> and <xref rid="Tab2" ref-type="table">2</xref>). Among these matched TDFs, 67 (50.8%) TDFs were up-regulated and 65 (49.2%) were down-regulated by B-toxicity. These TDFs were related to different biological processes such as cell transport (12.9%), lipid metabolism (2.3%), nucleic acid metabolism (12.9%), carbohydrate and energy metabolism (12.1%), protein and amino acid metabolism (25.0%), stress responses (6.1%), cell wall and cytoskeleton modification (6.8%), signal transduction (2.3%), other and unknown processes (19.7%) (Figure <xref rid="Fig4" ref-type="fig">4</xref>A). For <italic>C. sinensis</italic> leaves, 90 differentially expressed TDFs produced readable sequences (Tables <xref rid="Tab1" ref-type="table">1</xref> and <xref rid="Tab2" ref-type="table">2</xref>), 68 of which displayed homology to genes encoding known, putative, hypothetical, uncharacterized or unnamed proteins. The remaining 22 TDFs had no database matches. Of these matched TDFs, 31 (45.6%) TDFs increased and 37 (54.4%) decreased in response to B-toxicity. These TDFs were involved in cell transport (8.8%), lipid metabolism (4.4%), nucleic acid metabolism (13.2%), carbohydrate and energy metabolism (20.6%), protein and amino acid metabolism (25.0%), stress responses (7.4%), cell wall and cytoskeleton modification (2.9%), signal transduction (1.5%), other and unknown processes (16.2%) (Figure <xref rid="Fig4" ref-type="fig">4</xref>B).<table-wrap id="Tab2"><label>Table 2</label><caption><p><bold>Homologies of differentially expressed cDNA</bold>-<bold>AFLP fragments with known gene sequences in database using BLASTN algorithm along their expression patterns in B</bold>-<bold>toxic leaves of</bold><bold><italic>Citrus grandis</italic></bold><bold>and</bold><bold><italic>Citrus sinensis</italic></bold></p></caption><table frame="hsides" rules="groups"><thead><tr valign="top"><th rowspan="2"><bold>TDF #</bold></th><th rowspan="2"><bold>Size</bold><bold>(bp)</bold></th><th rowspan="2"><bold>Homology</bold></th><th rowspan="2"><bold>Organism origin</bold></th><th rowspan="2"><bold>E</bold>-<bold>value</bold></th><th rowspan="2"><bold>Similarity (%)</bold></th><th rowspan="2"><bold>Genebank ID</bold></th><th colspan="2"><bold>Ratio of BT/</bold><bold>CK</bold></th></tr><tr valign="top"><th><bold>CG</bold></th><th><bold>CS</bold></th></tr></thead><tbody><tr valign="top"><td colspan="3"><bold><italic>Carbohydrate and energy metabolism</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>143_2</td><td>280</td><td>Ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit precursor</td><td><italic>Citrus reticulata</italic></td><td>6.00E-49</td><td>93%</td><td>AAG49562.1</td><td>0</td><td></td></tr><tr valign="top"><td>251_1</td><td>329</td><td>Photosystem II 32 kDa protein (psbA)</td><td><italic>Dumortiera hirsuta</italic></td><td>1.00E-64</td><td>97%</td><td>AEI72217.1</td><td>0</td><td></td></tr><tr valign="top"><td>112_2</td><td>173</td><td>Chloroplast photosystem II oxygen-evolving complex 23 kDa polypeptide</td><td><italic>Cucumis sativus</italic></td><td>1.00E-18</td><td>75%</td><td>ABK55671.1</td><td>0</td><td>2.9</td></tr><tr valign="top"><td>239_4</td><td>223</td><td>NifU-like protein</td><td><italic>Medicago truncatula</italic></td><td>3.00E-17</td><td>87%</td><td>XP_003594958.1</td><td>0</td><td></td></tr><tr valign="top"><td>23_2</td><td>253</td><td>Glyceraldehyde-3-phosphate dehydrogenase B</td><td><italic>Arabidopsis thaliana</italic></td><td>3.00E-06</td><td>84%</td><td>NP_174996.1</td><td></td><td>+</td></tr><tr valign="top"><td>6_4</td><td>222</td><td>Rubisco activase</td><td><italic>A. thaliana</italic></td><td>1.00E-33</td><td>94%</td><td>BAF01986.1</td><td></td><td>0</td></tr><tr valign="top"><td>249_3</td><td>313</td><td>Sedoheptulose-1 7-bisphosphatase</td><td><italic>M. truncatula</italic></td><td>2.00E-48</td><td>97%</td><td>XP_003600853.1</td><td>+</td><td>+</td></tr><tr valign="top"><td>235_2</td><td>305</td><td>ADP-glucose pyrophosphorylase</td><td><italic>Pisum sativum</italic></td><td>5.00E-39</td><td>82%</td><td>CAA69978.1</td><td></td><td>0</td></tr><tr valign="top"><td>42_1</td><td>193</td><td>Starch branching enzyme I</td><td><italic>Ipomoea batatas</italic></td><td>1.00E-27</td><td>90%</td><td>BAE96953.1</td><td>0</td><td></td></tr><tr valign="top"><td>59_2</td><td>287</td><td>Glucose-1-phosphate adenylyltransferase large subunit 1</td><td><italic>A. thaliana</italic></td><td>2.00E-32</td><td>77%</td><td>NP_197423.1</td><td>0</td><td>0</td></tr><tr valign="top"><td>75_2</td><td>221</td><td>Citrate synthase</td><td><italic>Citrus maxima</italic></td><td>4.00E-34</td><td>97%</td><td>ADZ05826.1</td><td>2.8</td><td></td></tr><tr valign="top"><td>87_1</td><td>224</td><td>Pyruvate dehydrogenase E1 component subunit beta</td><td><italic>M. truncatula</italic></td><td>1.00E-26</td><td>83%</td><td>XP_003620963.1</td><td>+</td><td></td></tr><tr valign="top"><td>33_2</td><td>289</td><td>Aconitate hydratase 3</td><td><italic>Citrus clementina</italic></td><td>7.00E-50</td><td>94%</td><td>CBE71057.1</td><td>+</td><td></td></tr><tr valign="top"><td>161_3</td><td>257</td><td>2,3-bisphosphoglycerate- independent phosphoglycerate mutase</td><td><italic>Vitis amurensis</italic></td><td>1.00E-40</td><td>91%</td><td>ACI96093.1</td><td></td><td>+</td></tr><tr valign="top"><td>35_1</td><td>160</td><td>Plastidial pyruvate kinase 3</td><td><italic>A. thaliana</italic></td><td>6.00E-21</td><td>96%</td><td>NP_564402.1</td><td></td><td>0</td></tr><tr valign="top"><td>130_1</td><td>272</td><td>Aconitate hydratase 1</td><td><italic>Citrus clementina</italic></td><td>2.00E-31</td><td>98%</td><td>CBE71056.1</td><td></td><td>0</td></tr><tr valign="top"><td>171_2</td><td>328</td><td>Protochlorophyllide oxidoreductase C (PORC, AT1G03630)</td><td><italic>A. thaliana</italic></td><td>1.00E-43</td><td>89%</td><td>BAH57125.1</td><td>0</td><td>0</td></tr><tr valign="top"><td>5_1</td><td>192</td><td>Cytochrome P450</td><td><italic>Citrus sinensis</italic></td><td>2.00E-16</td><td>63%</td><td>AAL24049.1</td><td>+</td><td></td></tr><tr valign="top"><td>76_1</td><td>261</td><td>Cytochrome P450 like protein</td><td><italic>A. thaliana</italic></td><td>3.00E-29</td><td>68%</td><td>BAE99553.1</td><td>+</td><td></td></tr><tr valign="top"><td>237_2</td><td>258</td><td>1,3-beta-D-glucanase GH17_65</td><td><italic>Populus tremula</italic> × <italic>Populus tremuloides</italic></td><td>2.00E-31</td><td>78%</td><td>ADW08745.1</td><td></td><td>0</td></tr><tr valign="top"><td>233_5</td><td>216</td><td>Alpha-glucan water dikinase 1</td><td><italic>A. thaliana</italic></td><td>4.00E-14</td><td>82%</td><td>NP_563877.1</td><td>+</td><td>0</td></tr><tr valign="top"><td>57_3</td><td>176</td><td>UDP-D-glucuronate 4-epimerase 3</td><td><italic>A. thaliana</italic></td><td>1.00E-21</td><td>90%</td><td>NP_191922.1</td><td>0.3</td><td>+</td></tr><tr valign="top"><td>117_2</td><td>242</td><td>Rubredoxin family protein</td><td><italic>A. thaliana</italic></td><td>8.00E-24</td><td>81%</td><td>NP_568342.1</td><td></td><td>0</td></tr><tr valign="top"><td>121_1</td><td>179</td><td>Rieske iron-sulphur protein precursor</td><td><italic>Pinellia ternata</italic></td><td>6.00E-20</td><td>86%</td><td>CAM57108.1</td><td>+</td><td></td></tr><tr valign="top"><td colspan="3"><bold><italic>Lipid metabolism</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>10_1</td><td>282</td><td>Fatty acid hydroperoxide lyase</td><td><italic>Citrus aurantium</italic></td><td>2.00E-41</td><td>100%</td><td>ABI64149.1</td><td></td><td>0</td></tr><tr valign="top"><td>233_3</td><td>217</td><td>3-oxoacyl-reductase</td><td><italic>Zea mays</italic></td><td>2.00E-05</td><td>85%</td><td>NP_001167684.1</td><td></td><td>0</td></tr><tr valign="top"><td>195_1</td><td>321</td><td>Sugar-dependent1</td><td><italic>Arabidopsis lyrata subsp. lyrata</italic></td><td>3.00E-28</td><td>86%</td><td>XP_002871068.1</td><td></td><td>+</td></tr><tr valign="top"><td>8_1</td><td>232</td><td>Acyl carrier protein 1, chloroplastic-like</td><td><italic>Vitis vinifera</italic></td><td>6.4</td><td>42%</td><td>XP_003631979.1</td><td>0.4</td><td></td></tr><tr valign="top"><td>194_1</td><td>256</td><td>Alpha/beta-hydrolase domain-containing protein</td><td><italic>A. thaliana</italic></td><td>2.00E-34</td><td>72%</td><td>NP_181474.2</td><td>+</td><td></td></tr><tr valign="top"><td>186_4</td><td>276</td><td>Phospholipase-like protein (PEARLI 4) domain-containing protein</td><td><italic>A. thaliana</italic></td><td>7.00E-10</td><td>35%</td><td>NP_973499.1</td><td>+</td><td></td></tr><tr valign="top"><td colspan="3"><bold><italic>Nucleic acid metabolism</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>52_1</td><td>248</td><td>Spliceosomal protein U1A</td><td><italic>A. thaliana</italic></td><td>1.00E-24</td><td>69%</td><td>NP_182280.1</td><td>+</td><td></td></tr><tr valign="top"><td>49_1</td><td>337</td><td>Heat stress transcription factor B-2b</td><td><italic>M. truncatula</italic></td><td>8.00E-32</td><td>78%</td><td>XP_003611134.1</td><td>+</td><td></td></tr><tr valign="top"><td>72_4</td><td>171</td><td>Global transcription factor gro + A2</td><td><italic>A. thaliana</italic></td><td>2.00E-04</td><td>69%</td><td>NP_192575.3</td><td>+</td><td></td></tr><tr valign="top"><td>120_1</td><td>257</td><td>IAA13</td><td><italic>Solanum lycopersicum</italic></td><td>3.00E-30</td><td>67%</td><td>AEX00356.1</td><td>3.3</td><td></td></tr><tr valign="top"><td>44_1</td><td>307</td><td>Elongator complex protein 3</td><td><italic>A. thaliana</italic></td><td>4.00E-53</td><td>89%</td><td>NP_568725.1</td><td>+</td><td></td></tr><tr valign="top"><td>159_2</td><td>366</td><td>Flowering time control protein FPA (AT2G43410)</td><td><italic>A. thaliana</italic></td><td>0.14</td><td>32%</td><td>BAH56948.1</td><td>+</td><td></td></tr><tr valign="top"><td>164_1</td><td>285</td><td>ABA responsive element-binding protein</td><td><italic>Solanum torvum</italic></td><td>3.00E-10</td><td>84%</td><td>AFA37978.1</td><td>+</td><td>0</td></tr><tr valign="top"><td>73_2</td><td>255</td><td>Regulator of ribonuclease-like protein</td><td><italic>M. truncatula</italic></td><td>2.00E-08</td><td>83%</td><td>XP_003593378.1</td><td>+</td><td>+</td></tr><tr valign="top"><td>250_3</td><td>305</td><td>RNA recognition motif-containing protein</td><td><italic>A. thaliana</italic></td><td>7.00E-31</td><td>70%</td><td>NP_563946.1</td><td>0.4</td><td>2.7</td></tr><tr valign="top"><td>157_2</td><td>256</td><td>RNA recognition motif-containing protein</td><td><italic>A. thaliana</italic></td><td>3.00E-28</td><td>76%</td><td>NP_188119.1</td><td>0</td><td>+</td></tr><tr valign="top"><td>11_1</td><td>353</td><td>Putative RNA helicase MTR4</td><td><italic>A. thaliana</italic></td><td>1.00E-44</td><td>82%</td><td>NP_176185.1</td><td>0</td><td></td></tr><tr valign="top"><td>71_3</td><td>209</td><td>RNA helicase SDE3</td><td><italic>A. thaliana</italic></td><td>7.00E-24</td><td>71%</td><td>AAK40099.1</td><td>0</td><td>0</td></tr><tr valign="top"><td>186_1</td><td>395</td><td>Chromodomain-helicase-DNA-binding protein</td><td><italic>M. truncatula</italic></td><td>9.00E-56</td><td>73%</td><td>XP_003625728.1</td><td></td><td>0</td></tr><tr valign="top"><td>108_1</td><td>317</td><td>Receptor for activated C kinase 1B</td><td><italic>A. thaliana</italic></td><td>3.00E-40</td><td>87%</td><td>NP_175296.1</td><td></td><td>0</td></tr><tr valign="top"><td>67_4</td><td>195</td><td>Sequence-specific DNA binding transcription factor</td><td><italic>A. thaliana</italic></td><td>5.2</td><td>47%</td><td>NP_566386.1</td><td>0</td><td></td></tr><tr valign="top"><td>60_1</td><td>333</td><td>AT5g24120/MLE8_4</td><td><italic>A. thaliana</italic></td><td>9.00E-37</td><td>63%</td><td>AAK74018.1</td><td></td><td>+</td></tr><tr valign="top"><td>10_4</td><td>114</td><td>GRAS family transcription factor</td><td><italic>Populus trichocarpa</italic></td><td>2.00E-04</td><td>78%</td><td>XP_002310226.1</td><td>0</td><td></td></tr><tr valign="top"><td>22_3</td><td>248</td><td>MAF1-like protein</td><td><italic>Citrus sinensis</italic></td><td>2.00E-24</td><td>96%</td><td>AEV43358.1</td><td>0</td><td></td></tr><tr valign="top"><td>131_1</td><td>270</td><td>RNA-binding (RRM/RBD/RNP motifs) family protein</td><td><italic>A. thaliana</italic></td><td>7.00E-23</td><td>62%</td><td>NP_171616.1</td><td></td><td>7.3</td></tr><tr valign="top"><td>104_1</td><td>234</td><td>Zinc finger CCCH domain-containing protein</td><td><italic>M. truncatula</italic></td><td>1.00E-04</td><td>43%</td><td>XP_003605843.1</td><td>0</td><td></td></tr><tr valign="top"><td>68_2</td><td>217</td><td>F14N23.20</td><td><italic>A. thaliana</italic></td><td>3.00E-27</td><td>83%</td><td>AAD32882.1</td><td>0.3</td><td></td></tr><tr valign="top"><td colspan="3"><bold><italic>Protein and amino acid metabolism</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>236_1</td><td>312</td><td>Translation initiation factor IF-2, chloroplastic (AT1G17220)</td><td><italic>A. thaliana</italic></td><td>4.00E-45</td><td>85%</td><td>BAH20402.1</td><td>0</td><td></td></tr><tr valign="top"><td>117_4</td><td>174</td><td>Eukaryotic release factor 1-3</td><td><italic>Brassica oleracea var.botrytis</italic></td><td>3.00E-22</td><td>94%</td><td>ACZ71035.1</td><td>0</td><td></td></tr><tr valign="top"><td>93_3</td><td>193</td><td>EMB1241</td><td><italic>A.s lyrata subsp. lyrata</italic></td><td>5.00E-09</td><td>69%</td><td>XP_002873846.1</td><td>0.4</td><td></td></tr><tr valign="top"><td>73_3</td><td>201</td><td>Ankyrin repeat domain-containing protein</td><td><italic>M. truncatula</italic></td><td>5.00E-19</td><td>66%</td><td>XP_003614004.1</td><td>0.2</td><td></td></tr><tr valign="top"><td>179_4</td><td>274</td><td>50S ribosomal protein L15</td><td><italic>A. thaliana</italic></td><td>1.00E-18</td><td>80%</td><td>NP_189221.1</td><td>0</td><td></td></tr><tr valign="top"><td>105_1</td><td>216</td><td>30S ribosomal protein S17</td><td><italic>M. truncatula</italic></td><td>0.005</td><td>89%</td><td>XP_003604547.1</td><td>0</td><td>0</td></tr><tr valign="top"><td>99_6</td><td>165</td><td>60S ribosomal protein L6, putative</td><td><italic>A. thaliana</italic></td><td>2.00E-18</td><td>93%</td><td>AAM65875.1</td><td>0</td><td></td></tr><tr valign="top"><td>186_2</td><td>224</td><td>60S ribosomal protein L4-1</td><td><italic>A. thaliana</italic></td><td>3.00E-52</td><td>90%</td><td>NP_001030663.1</td><td>0</td><td></td></tr><tr valign="top"><td>129_2</td><td>253</td><td>60S ribosomal protein L23</td><td><italic>A. thaliana</italic></td><td>2.00E-74</td><td>97%</td><td>NP_001189805.1</td><td>+</td><td></td></tr><tr valign="top"><td>161_1</td><td>221</td><td>60S ribosomal protein L10B</td><td><italic>Hevea brasiliensis</italic></td><td>3.00E-27</td><td>83%</td><td>ADR71273.1</td><td>+</td><td></td></tr><tr valign="top"><td>93_2</td><td>210</td><td>SHEPHERD</td><td><italic>A. thaliana</italic></td><td>2.00E-26</td><td>86%</td><td>BAB86368.1</td><td>+</td><td></td></tr><tr valign="top"><td>98_1</td><td>272</td><td>Chaperonin 20</td><td><italic>A. thaliana</italic></td><td>2.00E-37</td><td>81%</td><td>NP_197572.1</td><td></td><td>0</td></tr><tr valign="top"><td>69_3</td><td>174</td><td>AT5G47880</td><td><italic>A. thaliana</italic></td><td>3.00E-20</td><td>92%</td><td>BAH19602.1</td><td></td><td>0</td></tr><tr valign="top"><td>23_4</td><td>208</td><td>MAP kinase</td><td><italic>A. thaliana</italic></td><td>1.00E-20</td><td>98%</td><td>CAB63149.1</td><td>0</td><td></td></tr><tr valign="top"><td>139_4</td><td>300</td><td>Putative leucine-rich repeat receptor-like protein kinase</td><td><italic>A. thaliana</italic></td><td>4.00E-25</td><td>55%</td><td>NP_200956.1</td><td>0</td><td></td></tr><tr valign="top"><td>72_1</td><td>238</td><td>CBL-interacting protein kinase 19</td><td><italic>Populus trichocarpa</italic></td><td>8.7</td><td>89%</td><td>ABJ91226.1</td><td>0</td><td></td></tr><tr valign="top"><td>39_3</td><td>200</td><td>At1g25390/F2J7_14</td><td><italic>A. thaliana</italic></td><td>3.00E-23</td><td>81%</td><td>AAK97715.1</td><td>0</td><td></td></tr><tr valign="top"><td>12_2</td><td>250</td><td>CDK activating kinase</td><td><italic>Nicotiana tabacum</italic></td><td>3.7</td><td>46%</td><td>BAF75824.1</td><td>+</td><td></td></tr><tr valign="top"><td>22_2</td><td>252</td><td>Serine/threonine protein kinase ATR</td><td><italic>M. truncatula</italic></td><td>6.00E-30</td><td>83%</td><td>XP_003592675.1</td><td>+</td><td></td></tr><tr valign="top"><td>235_3</td><td>285</td><td>Receptor-like protein kinase</td><td><italic>M. truncatula</italic></td><td>9.00E-11</td><td>57%</td><td>XP_003621121.1</td><td>+</td><td></td></tr><tr valign="top"><td>110_1</td><td>408</td><td>Receptor-like protein kinase</td><td><italic>A. thaliana</italic></td><td>2.00E-31</td><td>55%</td><td>BAA96958.1</td><td></td><td>0</td></tr><tr valign="top"><td>99_1</td><td>342</td><td>Protein phosphatase 2C (PP2C)</td><td><italic>Fagus sylvatica</italic></td><td>6.00E-30</td><td>71%</td><td>CAB90633.1</td><td>2.6</td><td>3.7</td></tr><tr valign="top"><td>99_2</td><td>273</td><td>C3H4 type zinc finger protein</td><td><italic>A. thaliana</italic></td><td>7.00E-28</td><td>64%</td><td>NP_194986.2</td><td>+</td><td></td></tr><tr valign="top"><td>54_1</td><td>318</td><td>AT5g57360/MSF19_2</td><td><italic>A. thaliana</italic></td><td>1.00E-45</td><td>75%</td><td>AAK64006.1</td><td>+</td><td></td></tr><tr valign="top"><td>57_1</td><td>246</td><td>E3 ligase SAP5</td><td><italic>A. thaliana</italic></td><td>2.00E-37</td><td>84%</td><td>NP_566429.1</td><td>+</td><td></td></tr><tr valign="top"><td>234_1</td><td>306</td><td>Root phototropism protein 2</td><td><italic>A. thaliana</italic></td><td>9.00E-29</td><td>60%</td><td>NP_001031446.1</td><td>2.8</td><td>3.4</td></tr><tr valign="top"><td>96_1</td><td>229</td><td>E3 ubiquitin-protein ligase BRE1-like protein</td><td><italic>M. truncatula</italic></td><td>2.8</td><td>29%</td><td>XP_003637493.1</td><td>0</td><td></td></tr><tr valign="top"><td>187_1</td><td>314</td><td>Skp1-like protein 1</td><td><italic>Prunus avium</italic></td><td>4.00E-51</td><td>85%</td><td>AFJ21662.1</td><td>0</td><td></td></tr><tr valign="top"><td>120_2</td><td>227</td><td>Polyubiquitin</td><td><italic>Cicer arietinum</italic></td><td>8.00E-39</td><td>100%</td><td>BAA76429.1</td><td>0.1</td><td></td></tr><tr valign="top"><td>158_2</td><td>313</td><td>Putative E3 ubiquitin-protein ligase XBAT31 isoform 2</td><td><italic>Vitis vinifera</italic></td><td>2.00E-18</td><td>63%</td><td>XP_002283974.1</td><td></td><td>+</td></tr><tr valign="top"><td>73_1</td><td>327</td><td>F-box family protein</td><td><italic>Citrus trifoliata</italic></td><td>4.00E-64</td><td>98%</td><td>ACL51019.1</td><td></td><td>0</td></tr><tr valign="top"><td>112_1</td><td>202</td><td>F-box with WD-40 2</td><td><italic>A. thaliana</italic></td><td>1.00E-04</td><td>81%</td><td>NP_567343.1</td><td></td><td>0</td></tr><tr valign="top"><td>38_3</td><td>212</td><td>Drought-inducible cysteine proteinase RD19A precursor</td><td><italic>A. thaliana</italic></td><td>1.00E-15</td><td>86%</td><td>BAD94010.1</td><td>6.0</td><td>0.3</td></tr><tr valign="top"><td>81_1</td><td>234</td><td>Metalloendopeptidase/zinc ion binding protein</td><td><italic>A. thaliana</italic></td><td>1.00E-31</td><td>84%</td><td>NP_568608.2</td><td>+</td><td></td></tr><tr valign="top"><td>38_4</td><td>261</td><td>Serine carboxypeptidase II-3</td><td><italic>M. truncatula</italic></td><td>7.00E-21</td><td>74%</td><td>XP_003589243.1</td><td>5.9</td><td></td></tr><tr valign="top"><td>73_4</td><td>143</td><td>Proteasome component (PCI) domain protein</td><td><italic>A. thaliana</italic></td><td>2.00E-07</td><td>69%</td><td>NP_850994.1</td><td></td><td>+</td></tr><tr valign="top"><td>240_1</td><td>359</td><td>RHOMBOID-like protein 3</td><td><italic>A. thaliana</italic></td><td>8.00E-38</td><td>65%</td><td>NP_196342.1</td><td></td><td>+</td></tr><tr valign="top"><td>39_1</td><td>248</td><td>Clp protease proteolytic subunit</td><td><italic>Citrus sinensis</italic></td><td>2.00E-29</td><td>100%</td><td>YP_740501.1</td><td>0</td><td></td></tr><tr valign="top"><td>145_1</td><td>319</td><td>Subtilase family protein</td><td><italic>A. thaliana</italic></td><td>3.00E-32</td><td>62%</td><td>NP_199378.1</td><td></td><td>0</td></tr><tr valign="top"><td>67_1</td><td>315</td><td>Aminopeptidase family protein</td><td><italic>A. thaliana</italic></td><td>2.00E-45</td><td>85%</td><td>NP_179997.1</td><td></td><td>0</td></tr><tr valign="top"><td>75_1</td><td>251</td><td>Papain family cysteine protease</td><td><italic>A. thaliana</italic></td><td>3.00E-26</td><td>85%</td><td>NP_567489.1</td><td></td><td>0</td></tr><tr valign="top"><td>138_4</td><td>320</td><td>AT4G01850</td><td><italic>A. thaliana</italic></td><td>3.00E-59</td><td>93%</td><td>BAH20274.1</td><td></td><td>+</td></tr><tr valign="top"><td>245_1</td><td>270</td><td>Methionine synthase</td><td><italic>Carica papaya</italic></td><td>2.00E-45</td><td>98%</td><td>ABS01352.1</td><td>0</td><td></td></tr><tr valign="top"><td>231_4</td><td>216</td><td>N-carbamoylputrescine amidase</td><td><italic>A. thaliana</italic></td><td>6.00E-10</td><td>76%</td><td>NP_565650.1</td><td>0.1</td><td></td></tr><tr valign="top"><td>61_2</td><td>289</td><td>2-oxoglutarate-dependent dioxygenase</td><td><italic>P. trichocarpa</italic></td><td>1.00E-07</td><td>74%</td><td>XP_002313083.1</td><td>+</td><td></td></tr><tr valign="top"><td>251_3</td><td>276</td><td>Cystathionine beta-synthase domain-containing protein</td><td><italic>A. thaliana</italic></td><td>8.00E-45</td><td>89%</td><td>NP_195409.1</td><td></td><td>0</td></tr><tr valign="top"><td colspan="3"><bold><italic>Stress responses</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>118_1</td><td>207</td><td>Inorganic pyrophosphatase 1</td><td><italic>A. thaliana</italic></td><td>2.00E-16</td><td>83%</td><td>NP_565052.1</td><td>0</td><td>3.3</td></tr><tr valign="top"><td>148_2</td><td>317</td><td>Nudix hydrolase 19</td><td><italic>A. thaliana</italic></td><td>2.00E-48</td><td>78%</td><td>NP_197507.1</td><td>0</td><td>+</td></tr><tr valign="top"><td>59_1</td><td>346</td><td>Fe (II)/ascorbate oxidase family protein SRG1</td><td><italic>A. thaliana</italic></td><td>2.00E-16</td><td>71%</td><td>NP_173145.1</td><td></td><td>0</td></tr><tr valign="top"><td>137_2</td><td>156</td><td>Thioredoxin superfamily protein</td><td><italic>A. thaliana</italic></td><td>3.00E-10</td><td>58%</td><td>NP_198706.1</td><td>+</td><td></td></tr><tr valign="top"><td>68_3</td><td>146</td><td>Thioredoxin superfamily protein</td><td><italic>A. thaliana</italic></td><td>3.00E-07</td><td>59%</td><td>NP_201385.2</td><td>0.1</td><td></td></tr><tr valign="top"><td>2_1</td><td>276</td><td>Group 5 late embryogenesis abundant protein (LEA5)</td><td><italic>Citrus unshiu</italic></td><td>1.00E-35</td><td>94%</td><td>ABD93882.1</td><td>3.0</td><td></td></tr><tr valign="top"><td>125_1</td><td>389</td><td>Thaumatin-like protein 1</td><td>Apple tree</td><td>9.00E-48</td><td>69%</td><td>JC7201</td><td>+</td><td></td></tr><tr valign="top"><td>99_5</td><td>190</td><td>Protein sodium-and lithium-tolerant 1</td><td><italic>A. thaliana</italic></td><td>1.00E-23</td><td>92%</td><td>NP_973625.1</td><td>0</td><td></td></tr><tr valign="top"><td>104_3</td><td>171</td><td>Transducin/WD40 domain-containing protein (AtATG18a, AT3G62770)</td><td><italic>A. thaliana</italic></td><td>3.00E-20</td><td>94%</td><td>NP_001030918.4</td><td></td><td>0</td></tr><tr valign="top"><td>109_1</td><td>257</td><td>Cold regulated 314 thylakoid membrane 2</td><td><italic>A. thaliana</italic></td><td>1.00E-19</td><td>56%</td><td>NP_564327.1</td><td></td><td>0</td></tr><tr valign="top"><td>150_2</td><td>238</td><td>Universal stress protein A-like protein</td><td><italic>M. truncatula</italic></td><td>4.00E-27</td><td>71%</td><td>XP_003591417.1</td><td>0.2</td><td></td></tr><tr valign="top"><td colspan="4"><bold><italic>Signal transduction</italic></bold></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>182_2</td><td>117</td><td>Signal recognition particle 54 kDa protein 2</td><td><italic>Solanum lycopersicum</italic></td><td>7.00E-07</td><td>93%</td><td>NP_001234428.1</td><td>0</td><td></td></tr><tr valign="top"><td>108_2</td><td>257</td><td>14-3-3 protein</td><td><italic>Dimocarpus longan</italic></td><td>6.00E-38</td><td>93%</td><td>ACK76233.1</td><td>0</td><td></td></tr><tr valign="top"><td>200_1</td><td>240</td><td>Heterotrimeric GTP-binding protein subunit beta 1</td><td><italic>Nicotiana tabacum</italic></td><td>3.00E-39</td><td>94%</td><td>AAG12330.1</td><td>0</td><td></td></tr><tr valign="top"><td>70_2</td><td>252</td><td>Pseudo-response regulator 5</td><td><italic>Castanea sativa</italic></td><td>5.00E-12</td><td>86%</td><td>ABV53464.1</td><td></td><td>+</td></tr><tr valign="top"><td colspan="2"><bold><italic>Cell transport</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>26_1</td><td>342</td><td>H<sup>+</sup>-ATPase 6, plasma membrane-type</td><td><italic>A. thaliana</italic></td><td>1.00E-38</td><td>97%</td><td>NP_178762.1</td><td>+</td><td></td></tr><tr valign="top"><td>124_3</td><td>166</td><td>Calcium-transporting ATPase 1, endoplasmic reticulum-type (ECA1)</td><td><italic>A. thaliana</italic></td><td>2.00E-14</td><td>83%</td><td>NP_172259.1</td><td>3.1</td><td></td></tr><tr valign="top"><td>66_1</td><td>177</td><td>Heavy metal ATPase</td><td><italic>P. trichocarpa</italic></td><td>4.00E-15</td><td>78%</td><td>XP_002303580.1</td><td>+</td><td></td></tr><tr valign="top"><td>97_1</td><td>201</td><td>Proton pump-interactor 1 (PPI1, AT4G27500)</td><td><italic>A. thaliana</italic></td><td>3.00E-12</td><td>56%</td><td>BAH19433.1</td><td>+</td><td></td></tr><tr valign="top"><td>53_1</td><td>340</td><td>ABC transporter G family member 40</td><td><italic>A. thaliana</italic></td><td>9.00E-35</td><td>67%</td><td>NP_173005.1</td><td>+</td><td></td></tr><tr valign="top"><td>210_1</td><td>247</td><td>Copper transporter</td><td><italic>P. trichocarpa</italic></td><td>2.00E-15</td><td>64%</td><td>XP_002298334.1</td><td>+</td><td></td></tr><tr valign="top"><td>178_1</td><td>297</td><td>Cyclic nucleotide-gated ion channel 1</td><td><italic>A. thaliana</italic></td><td>0.002</td><td>50%</td><td>NP_200125.1</td><td>+</td><td></td></tr><tr valign="top"><td>49_3</td><td>252</td><td>Vacuolar-sorting receptor 3</td><td><italic>A. thaliana</italic></td><td>1.00E-40</td><td>77%</td><td>NP_179081.1</td><td>+</td><td></td></tr><tr valign="top"><td>137_1</td><td>249</td><td>Vacuolar protein-sorting-associated protein 37-1</td><td><italic>A. thaliana</italic></td><td>0.48</td><td>63%</td><td>NP_190880.1</td><td>+</td><td></td></tr><tr valign="top"><td>63_1</td><td>357</td><td>Vesicle-associated membrane protein-associated protein</td><td><italic>M. truncatula</italic></td><td>3.00E-05</td><td>70%</td><td>XP_003608721.1</td><td>+</td><td></td></tr><tr valign="top"><td>51_1</td><td>316</td><td>SecY protein transport family protein</td><td><italic>A. thaliana</italic></td><td>2.00E-51</td><td>87%</td><td>NP_174225.2</td><td>+</td><td></td></tr><tr valign="top"><td>250_2</td><td>263</td><td>Fat-free-like protein</td><td><italic>M. truncatula</italic></td><td>1.00E-32</td><td>82%</td><td>XP_003591407.1</td><td>+</td><td></td></tr><tr valign="top"><td>79_2</td><td>237</td><td>Non-specific lipid-transfer protein</td><td><italic>M. truncatula</italic></td><td>1.00E-04</td><td>53%</td><td>XP_003610781.1</td><td>2.5</td><td></td></tr><tr valign="top"><td>67_3</td><td>268</td><td>Sieve element occlusion protein 1</td><td><italic>Nicotiana tabacum</italic></td><td>6.00E-23</td><td>65%</td><td>AFN06072.1</td><td>+</td><td>+</td></tr><tr valign="top"><td>89_2</td><td>230</td><td>AT5g24810/F6A4_20</td><td><italic>A. thaliana</italic></td><td>1.00E-04</td><td>75%</td><td>AAK82520.1</td><td>0</td><td></td></tr><tr valign="top"><td>6_1</td><td>368</td><td>Protein transport protein SEC61 gamma subunit</td><td><italic>Zea mays</italic></td><td>2.00E-04</td><td>92%</td><td>NP_001150911.1</td><td>0</td><td></td></tr><tr valign="top"><td>249_2</td><td>370</td><td>Putative beta-subunit of adaptor protein complex 3, PAT2</td><td><italic>A. thaliana</italic></td><td>2.00E-15</td><td>42%</td><td>NP_567022.1</td><td>0</td><td>0</td></tr><tr valign="top"><td>61_1</td><td>228</td><td>Sugar transporter ERD6-like 5</td><td><italic>A. thaliana</italic></td><td>7.00E-15</td><td>57%</td><td>NP_564665.3</td><td></td><td>0</td></tr><tr valign="top"><td>179_2</td><td>225</td><td>Metal tolerance protein</td><td><italic>P. trichocarpa</italic></td><td>6.00E-26</td><td>70%</td><td>XP_002312066.1</td><td></td><td>0</td></tr><tr valign="top"><td>51_4</td><td>221</td><td>Kinesin-related protein</td><td><italic>M. truncatula</italic></td><td>0.38</td><td>35%</td><td>XP_003612133.1</td><td></td><td>+</td></tr><tr valign="top"><td>36_2</td><td>319</td><td>Bidirectional sugar transporter SWEET7</td><td><italic>A. thaliana</italic></td><td>5.00E-08</td><td>60%</td><td>NP_567366.1</td><td></td><td>+</td></tr><tr valign="top"><td colspan="3"><bold><italic>Cell wall and cytoskeleton modification</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>49_4</td><td>210</td><td>Caffeic acid 3-O-methyltransferase</td><td><italic>M. truncatula</italic></td><td>9.00E-23</td><td>68%</td><td>XP_003602597.1</td><td></td><td>0</td></tr><tr valign="top"><td>125_2</td><td>145</td><td>Caffeic acid O-methyltransferase 3</td><td><italic>Gossypium hirsutum</italic></td><td>2.00E-05</td><td>55%</td><td>ACZ06242.1</td><td>0.2</td><td></td></tr><tr valign="top"><td>10_3</td><td>274</td><td>Chitinase</td><td><italic>Citrus sinensis</italic></td><td>3.00E-54</td><td>94%</td><td>CAA93847.1</td><td>0</td><td>0</td></tr><tr valign="top"><td>249_4</td><td>217</td><td>Cellulose synthase</td><td><italic>Populus tremuloides</italic></td><td>1.00E-20</td><td>83%</td><td>AAO25581.1</td><td>0.2</td><td></td></tr><tr valign="top"><td>33_3</td><td>249</td><td>O-methyltransferase 1</td><td><italic>A. thaliana</italic></td><td>1.00E-33</td><td>74%</td><td>AAB96879.1</td><td>+</td><td></td></tr><tr valign="top"><td>241_1</td><td>326</td><td>LIM domain-containing protein</td><td><italic>A. thaliana</italic></td><td>1.00E-64</td><td>94%</td><td>NP_195404.6</td><td>+</td><td></td></tr><tr valign="top"><td>124_2</td><td>385</td><td>UDP-glucose flavonoid 7-O-glucosyltransferase</td><td><italic>M. truncatula</italic></td><td>4.00E-12</td><td>73%</td><td>XP_003629628.1</td><td>+</td><td></td></tr><tr valign="top"><td>3_3</td><td>225</td><td>UDP-glucosyltransferase family 1 protein</td><td><italic>Citrus sinensis</italic></td><td>6.00E-36</td><td>96%</td><td>ACS87993.1</td><td>+</td><td></td></tr><tr valign="top"><td>70_4</td><td>176</td><td>Limonoid UDP-glucosyltransferase</td><td><italic>Citrus sinensis</italic></td><td>2.00E-26</td><td>98%</td><td>ACD14147.1</td><td>+</td><td></td></tr><tr valign="top"><td>63_2</td><td>228</td><td>Putative glucosyltransferase</td><td><italic>A. thaliana</italic></td><td>2.00E-20</td><td>63%</td><td>AAM61749.1</td><td>3.9</td><td></td></tr><tr valign="top"><td colspan="3"><bold><italic>Other and unknown processes</italic></bold></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr valign="top"><td>229_4</td><td>181</td><td>Phytoene synthase</td><td><italic>Citrus unshiu</italic></td><td>1.00E-26</td><td>95%</td><td>AAF33237.1</td><td>0</td><td></td></tr><tr valign="top"><td>231_1</td><td>316</td><td>Strictosidine synthase family protein</td><td><italic>A. thaliana</italic></td><td>2.00E-28</td><td>68%</td><td>NP_191262.2</td><td>0.4</td><td>2.6</td></tr><tr valign="top"><td>72_3</td><td>194</td><td>Calcium-dependent lipid-binding domain-containing protein</td><td><italic>A. thaliana</italic></td><td>8.00E-19</td><td>78%</td><td>NP_564576.1</td><td>+</td><td>+</td></tr><tr valign="top"><td>135_2</td><td>335</td><td>Oxidoreductase family protein</td><td><italic>Arabidopsis lyrata subsp.lyrata</italic></td><td>3.00E-40</td><td>65%</td><td>XP_002874584.1</td><td></td><td>0</td></tr><tr valign="top"><td>5_2</td><td>262</td><td>Alkaline-phosphatase-like protein</td><td><italic>A. thaliana</italic></td><td>7.00E-44</td><td>89%</td><td>NP_194697.1</td><td>0</td><td></td></tr><tr valign="top"><td>10_5</td><td>147</td><td>Protein tolB</td><td><italic>M. truncatula</italic></td><td>2.00E-06</td><td>55%</td><td>XP_003630471.1</td><td>+</td><td></td></tr><tr valign="top"><td>231_2</td><td>285</td><td>Cofactor of nitrate reductase and xanthine dehydrogenase 3</td><td><italic>A. thaliana</italic></td><td>5.00E-35</td><td>83%</td><td>NP_171636.1</td><td></td><td>3.9</td></tr><tr valign="top"><td>51_3</td><td>256</td><td>Neutral/alkaline non-lysosomal ceramidase</td><td><italic>A. thaliana</italic></td><td>3.00E-14</td><td>71%</td><td>NP_172218.1</td><td></td><td>0.5</td></tr><tr valign="top"><td>229_2</td><td>207</td><td>PQ-loop repeat family protein</td><td><italic>A. lyrata subsp. lyrata</italic></td><td>2.00E-22</td><td>74%</td><td>XP_002870687.1</td><td>+</td><td></td></tr><tr valign="top"><td>71_4</td><td>206</td><td>Metallo-beta-lactamase domain-containing protein</td><td><italic>A. thaliana</italic></td><td>9.00E-19</td><td>66%</td><td>NP_564334.1</td><td>+</td><td></td></tr><tr valign="top"><td>117_3</td><td>214</td><td>Oligosaccharyltransferase complex/magnesium transporter family protein</td><td><italic>A. thaliana</italic></td><td>5.00E-17</td><td>60%</td><td>NP_176372.1</td><td>0</td><td></td></tr><tr valign="top"><td>146_3</td><td>337</td><td>Mitochondrial protein, putative</td><td><italic>M. truncatula</italic></td><td>1.00E-24</td><td>74%</td><td>XP_003588355.1</td><td>0.4</td><td>0.3</td></tr><tr valign="top"><td>20_1</td><td>287</td><td>AT1G16560</td><td><italic>A. thaliana</italic></td><td>2.00E-42</td><td>74%</td><td>BAH19866.1</td><td>+</td><td></td></tr><tr valign="top"><td>117_1</td><td>338</td><td>At2g27385</td><td><italic>A. lyrata subsp. lyrata</italic></td><td>8.00E-15</td><td>91%</td><td>XP_002880912.1</td><td>0.2</td><td></td></tr><tr valign="top"><td>173_1</td><td>290</td><td>SOUL heme-binding protein</td><td><italic>A. thaliana</italic></td><td>1.00E-40</td><td>90%</td><td>NP_197514.2</td><td>0</td><td></td></tr><tr valign="top"><td>122_1</td><td>166</td><td>AT-LS1 product</td><td><italic>A. thaliana</italic></td><td>2.00E-21</td><td>86%</td><td>CAA41632.1</td><td>0</td><td></td></tr><tr valign="top"><td>77_2</td><td>231</td><td>Alpha/beta-hydrolase family protein</td><td><italic>A. thaliana</italic></td><td>3.00E-36</td><td>94%</td><td>NP_196943.1</td><td>1.8</td><td></td></tr><tr valign="top"><td>99_3</td><td>265</td><td>Conserved hypothetical protein</td><td><italic>Ricinus communis</italic></td><td>0.069</td><td>44%</td><td>XP_002511001.1</td><td>0</td><td>+</td></tr><tr valign="top"><td>229_1</td><td>271</td><td>Conserved hypothetical protein</td><td><italic>R. communis</italic></td><td>2.00E-09</td><td>90%</td><td>XP_002532497.1</td><td>0</td><td></td></tr><tr valign="top"><td>70_1</td><td>267</td><td>Predicted protein</td><td><italic>Micromonas pusilla CCMP1545</italic></td><td>3.00E-49</td><td>94%</td><td>XP_003064993.1</td><td>+</td><td>+</td></tr><tr valign="top"><td>123_1</td><td>364</td><td>PREDICTED: exportin-4-like</td><td><italic>Vitis vinifera</italic></td><td>9.00E-47</td><td>81%</td><td>XP_002266608.2</td><td>+</td><td></td></tr><tr valign="top"><td>23_1</td><td>308</td><td>Predicted protein</td><td><italic>P. trichocarpa</italic></td><td>0.062</td><td>34%</td><td>XP_002317402.1</td><td>+</td><td></td></tr><tr valign="top"><td>232_2</td><td>246</td><td>Predicted protein</td><td><italic>P. trichocarpa</italic></td><td>5.00E-12</td><td>48%</td><td>XP_002319603.1</td><td>0.1</td><td></td></tr><tr valign="top"><td>237_1</td><td>265</td><td>PREDICTED: uncharacterized protein LOC100776190</td><td><italic>Glycine max</italic></td><td>5.8</td><td>36%</td><td>XP_003524378.1</td><td>0</td><td></td></tr><tr valign="top"><td>242_1</td><td>245</td><td>PREDICTED: uncharacterized protein LOC100789831</td><td><italic>G. max</italic></td><td>2.00E-07</td><td>60%</td><td>XP_003520084.1</td><td>+</td><td></td></tr><tr valign="top"><td>69_2</td><td>244</td><td>PREDICTED: uncharacterized protein LOC100853355</td><td><italic>Vitis vinifera</italic></td><td>0.008</td><td>49%</td><td>XP_003634177.1</td><td>0</td><td></td></tr><tr valign="top"><td>130_2</td><td>210</td><td>Uncharacterized protein</td><td><italic>A. thaliana</italic></td><td>6.00E-21</td><td>79%</td><td>NP_176682.1</td><td></td><td>1.7</td></tr><tr valign="top"><td>252_1</td><td>301</td><td>Uncharacterized protein</td><td><italic>A. thaliana</italic></td><td>8.00E-16</td><td>56%</td><td>NP_001031080.1</td><td>0</td><td></td></tr><tr valign="top"><td>97_2</td><td>163</td><td>Unnamed protein product</td><td><italic>Vitis vinifera</italic></td><td>0.079</td><td>42%</td><td>CBI21631.3</td><td>0</td><td>7.0</td></tr><tr valign="top"><td>91_2</td><td>270</td><td>Hypothetical protein</td><td><italic>A. thaliana</italic></td><td>0.19</td><td>54%</td><td>AAD21766.1</td><td></td><td>3.9</td></tr><tr valign="top"><td>9_1</td><td>255</td><td>Hypothetical protein MTR_5g051130</td><td><italic>M. truncatula</italic></td><td>1.00E-11</td><td>100%</td><td>XP_003614394.1</td><td>+</td><td></td></tr></tbody></table><table-wrap-foot><p>Expression ratio: 0 means TDFs were only detected in control leaves; + means TDF were only detected in the B-toxic leaves. #: Number; BT: B-toxicity; CK: Control; CG: <italic>C. grandis</italic>; CS: <italic>C. sinensis</italic>. Functional classification was performed based on the information reported for each sequence by The Gene Ontology (<ext-link ext-link-type="uri" xlink:href="http://amigo1.geneontology.org/cgi-bin/amigo/blast.cgi">http://amigo1.geneontology.org/cgi-bin/amigo/blast.cgi</ext-link>) and Uniprot (<ext-link ext-link-type="uri" xlink:href="http://www.uniprot.org/">http://www.uniprot.org/</ext-link>). Relative expression ratio was obtained by gel image analysis, which was performed with PDQuest version 8.0.1 (Bio-Rad, Hercules, CA, USA).</p></table-wrap-foot></table-wrap><fig id="Fig4"><label>Figure 4</label><caption><p><bold>Functional classification of differentially expressed TDFs under B</bold>-<bold>toxicity in</bold><bold><italic>Citrus grandis</italic></bold><bold>(A)</bold><bold>and</bold><bold><italic>Citrus sinensis</italic></bold><bold>leaves</bold><bold>(B).</bold> Functional classification was performed based on the information reported for each sequence by The Gene Ontology (<ext-link ext-link-type="uri" xlink:href="http://amigo1.geneontology.org/cgi-bin/amigo/blast.cgi">http://amigo1.geneontology.org/cgi-bin/amigo/blast.cgi</ext-link>) and Uniprot (<ext-link ext-link-type="uri" xlink:href="http://www.uniprot.org/">http://www.uniprot.org/</ext-link>).</p></caption><graphic xlink:href="12870_2014_284_Fig4_HTML" id="MO4"></graphic></fig></p></sec><sec id="Sec6"><title>Validation of cDNA-AFLP data using qRT-PCR</title><p>In this study, nine TDFs from <italic>C. sinensis</italic> leaves and nine TDFs from <italic>C. grandis</italic> ones were selected for qRT-PCR analysis in order to validate their expression patterns obtained by cDNA-AFLP analysis. Except for two TDFs (i.e., TDFs #187_1 and 195_1), the expression profiles of all the TDFs obtained by qRT-PCR were in agreement with the expression patterns produced by cDNA-AFLP (Figure <xref rid="Fig5" ref-type="fig">5</xref>). This technique was thus validated in 88.9% of cases. In addition to gene family complexity, the changes in the intensity of individual bands in the cDNA-AFLP gels might be responsible for the discrepancies between qRT-PCR and cDNA-AFLP analysis.<fig id="Fig5"><label>Figure 5</label><caption><p><bold>Effects of B</bold>-<bold>toxicity on gene expression of</bold><bold><italic>Citrus grandis</italic></bold><bold>(A)</bold><bold>and</bold><bold><italic>Citrus sinensis</italic></bold><bold>(B)</bold><bold>leaves.</bold><bold>(A)</bold> Relative expression levels of genes encoding chitinase (TDF #10_3), H<sup>+</sup>-ATPase 6 (TDF #26-1), secY protein transport family protein (TDF #51_1), pyruvate dehydrogenase E1 component subunit β (TDF #87-1), putative leucine-rich repeat receptor-like protein kinase (TDF #139_4), Rubisco small subunit precursor (TDF #143-2), PORC (TDF #171_2), Skp1-like protein 1 (TDF #187_1) and LIM domain-containing protein (TDF #241_1). <bold>(B)</bold> Relative expression levels of genes encoding fatty acid hydroperoxide lyase (TDF #10_1), chitinase (TDF #10_3), glyceraldehyde-3-phosphate dehydrogenase B (TDF #23-2), F-box family protein (TDF #73-1), AT4G01850 (TDF #138_4), subtilase family protein (TDF #145_1), Nudix hydrolase 19 (TDF #148_2), PORC (TDF #171_2) and sugar-dependent1 (TDF #195_1). Bars represent means ± SE (n =3). Different letters above the bars indicate a significant difference at <italic>P</italic> <0.05.</p></caption><graphic xlink:href="12870_2014_284_Fig5_HTML" id="MO5"></graphic></fig></p></sec></sec><sec id="Sec7" sec-type="discussion"><title>Discussion</title><sec id="Sec8"><title><italic>C. sinensis</italic> displayed higher B-tolerance than <italic>C. grandis</italic></title><p>Our results showed that the effects of B-toxicity on plant growth (Figure <xref rid="Fig1" ref-type="fig">1</xref>A-C), and leaf gas exchange, pigments, total soluble protein, MDA (Figure <xref rid="Fig3" ref-type="fig">3</xref>) and P (Figure <xref rid="Fig2" ref-type="fig">2</xref>C) were more pronounced in <italic>C. grandis</italic> than in <italic>C. sinensis</italic> seedlings, meaning that <italic>C. sinensis</italic> has higher B-tolerance than <italic>C. grandis</italic>. The present work, like that of the previous workers [<xref ref-type="bibr" rid="CR8">8</xref>,<xref ref-type="bibr" rid="CR13">13</xref>,<xref ref-type="bibr" rid="CR15">15</xref>], indicates that the major of B in B-toxic citrus plants was accumulated in the leaves (Figure <xref rid="Fig2" ref-type="fig">2</xref>A and B). As shown in Figure <xref rid="Fig2" ref-type="fig">2</xref>B, B concentration was not lower in <italic>C. sinensis</italic> than in <italic>C. grandis</italic> leaves regardless of B concentration in the nutrient solution, indicating that <italic>C. sinensis</italic> leaves may tolerate higher level of B. Similar result has been obtained by Huang et al. [<xref ref-type="bibr" rid="CR13">13</xref>]. Here we isolated 67 up-regulated and 65 down-regulated TDFs from B-toxic <italic>C. grandis</italic> leaves, whilst only 31 up-regulated and 37 down-regulated TDFs from B-toxic <italic>C. sinensis</italic> ones (Figure <xref rid="Fig4" ref-type="fig">4</xref>), suggesting that B-toxicity affects <italic>C. sinensis</italic> leaves gene expression less than <italic>C. grandis</italic> ones. These data also support above inference that <italic>C. sinensis</italic> leaves may tolerate higher level of B.</p><p>We found that CO<sub>2</sub> assimilation was lower in toxic leaves than in control leaves, while stomatal conductance was not lower in the former (Figure <xref rid="Fig3" ref-type="fig">3</xref>A-C), implies that B-toxicity-induced inhibition of CO<sub>2</sub> assimilation in two citrus species is primarily due to non-stomatal factors. Similar results have been obtained on B-toxic <italic>C. grandis</italic> and <italic>C. sinensis</italic> [<xref ref-type="bibr" rid="CR13">13</xref>,<xref ref-type="bibr" rid="CR14">14</xref>], ‘Navelina’ orange and ‘Clementine’ mandarin plants grafted on sour orange and Swingle citrumelo rootstocks [<xref ref-type="bibr" rid="CR11">11</xref>,<xref ref-type="bibr" rid="CR12">12</xref>], Newhall and Skagg’s Bonanza navel orange plants grafted on Carrizo citrange and trifoliate orange [<xref ref-type="bibr" rid="CR9">9</xref>].</p></sec><sec id="Sec9"><title>Leaf carbohydrate and energy metabolism</title><p>Since B-toxicity decreased CO<sub>2</sub> assimilation (Figure <xref rid="Fig3" ref-type="fig">3</xref>A), genes involved in photosynthesis and related biological processes might be affected by B-toxicity. As expected, 16 TDFs in <italic>C. grandis</italic> leaves and 14 TDFs in <italic>C. sinensis</italic> ones related to carbohydrate and energy metabolism were altered under B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref> and Figure <xref rid="Fig4" ref-type="fig">4</xref>). We found that B-toxicity decreased the transcript level of ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) small subunit precursor (TDF #143_2) gene in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), which agrees with the previous report that B-toxicity decreased the activity of Rubisco in <italic>C. grandis</italic> leaves [<xref ref-type="bibr" rid="CR14">14</xref>]. Hudson et al. showed that the reduction of Rubisco concentration by anti-small subunit led to decreased photosynthesis in transgenic tobacco plants, but unchanged stomatal conductance [<xref ref-type="bibr" rid="CR16">16</xref>]. Also, the mRNA abundances of photosystem II (PSII) 32 kDa protein (PsbA, TDF #251_1), chloroplast PSII oxygen-evolving complex 23 kDa polypeptide (TDF #112_2) and NifU-like protein (TDF #239_4) genes were down-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). Khan et al. reported that <italic>PsbA</italic> knockout tobacco plants lacked PSII activity, accompanied by promoted senescence [<xref ref-type="bibr" rid="CR17">17</xref>]. By using differential RNA interference (RNAi), Ishihara et al. demonstrated that PSII activity was linearly correlated with the total amount of PsbP (PSII 23 kDa protein) [<xref ref-type="bibr" rid="CR18">18</xref>]. Ifuku et al. reported that PsbP is essential for the regulation and stabilization of PSII in higher plants [<xref ref-type="bibr" rid="CR19">19</xref>]. Yabe et al. proposed that <italic>Arabidopsis</italic> chloroplastic NifU-like protein, which can act as a Fe-S cluster scaffold protein, was required for biogenesis of ferredoxin and photosystem I (PSI) [<xref ref-type="bibr" rid="CR20">20</xref>]. B-toxicity-induced decreases in the transcript levels of PsbA, chloroplast PSII oxygen-evolving complex 23 kDa polypeptide and NifU-like protein genes agree with our report that B-toxicity impaired the whole photosynthetic electron transport from PSII donor side up to the reduction of end acceptors of PSI in <italic>C. grandis</italic> leaves [<xref ref-type="bibr" rid="CR14">14</xref>]. By contrast, B-toxicity increased the transcript levels of chloroplast PSII oxygen-evolving complex 23 kDa polypeptide (TDF #112_2) and glyceraldehyde-3-phosphate dehydrogenase B (TDE #23_2) in <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). NADP-glyceraldehyde-3-phosphate dehydrogenase is one of the two chloroplast enzymes which catalyze the reduction of 3-phosphoglycerate to triose phosphate [<xref ref-type="bibr" rid="CR21">21</xref>]. However, the expression of Rubisco activase (TDF #6_4) gene in <italic>C. sinensis</italic> leaves decreased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>). Generally speaking, B-toxic <italic>C. sinensis</italic> leaves had higher expression levels of photosynthetic genes than B-toxic <italic>C. grandis</italic> ones. This might be responsible for the greater decrease in CO<sub>2</sub> assimilation in B-toxic <italic>C. grandis</italic> leaves compared with B-toxic <italic>C. sinensis</italic> ones. It is noteworthy that the mRNA level of gene encoding sedoheptulose-1,7-bisphosphatase (SBPase, TDF #249_3), a key factor for the RuBP regeneration, was up-regulated in B-toxic leaves of the two citrus species (Table <xref rid="Tab2" ref-type="table">2</xref>). Harrison et al. showed that a small decrease in SBPase activity caused a decline in CO<sub>2</sub> assimilation by reducing the capacity for RuBP regeneration [<xref ref-type="bibr" rid="CR22">22</xref>]. Lefebvre et al. observed that transgenic tobacco plants over-expressing <italic>SBPase</italic> had enhanced photosynthesis and growth from an early stage in development [<xref ref-type="bibr" rid="CR23">23</xref>]. Wang reported that transgenic tomato plants over-expressing <italic>SBPase</italic> were more tolerance to low temperature and had higher photosynthetic capacity under low temperature [<xref ref-type="bibr" rid="CR24">24</xref>]. Therefore, the up-regulation of <italic>SBPase</italic> might be an adaptive response to B-toxicity.</p><p>As shown in Table <xref rid="Tab2" ref-type="table">2</xref>, B-toxicity decreased leaf expression levels of three genes [i.e., ADP-glucose pyrophosphorylase (TDF #235_2) in <italic>C. sinensis</italic>, starch branching enzyme I (TDF #42_1) in <italic>C. grandis</italic> and glucose-1-phosphate adenylyltransferase large subunit 1 (TDF #59_2) in the two citrus species] related to starch biosynthesis, which agrees with the previous report that B-toxicity decreased starch concentration in <italic>C. grandis</italic> leaves [<xref ref-type="bibr" rid="CR14">14</xref>].</p><p>B-toxicity increased the mRNA levels of three genes encoding citrate synthase (TDF #75-2), pyruvate dehydrogenase E1 component subunit beta (TDF #87_1) and aconitate hydratase 3 (TDF #33-2) in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), indicating that tricarboxylic acid cycle might be up-regulated in B-toxic <italic>C. grandis</italic> leaves. Similarly, the transcript level of a glycolysis gene encoding 2,3-bisphosphoglycerate-independent phosphoglycerate mutase (TDF #161_3) was enhanced in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). However, the mRNA levels of plastidial pyruvate kinase 3 (TDF #35_1) and aconitate hydratase 1 (TDF #33_2) genes were reduced in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). There is evidence showing that plastidic pyruvate kinase plays a key role in fatty acid synthesis by controlling the supply of ATP and pyruvate for <italic>de novo</italic> fatty acid synthesis in plastids [<xref ref-type="bibr" rid="CR25">25</xref>]. Thus, the fatty acid metabolism in B-toxic <italic>C. sinensis</italic> leaves might be impaired due to decreased plastidic pyruvate kinase.</p><p>In <italic>Arabidopsis</italic>, three NADPH: protochlorophyllide oxidoreductases (PORs), denoted as PORA, PORB, and PORC participate in mediating the light-dependent protochlorophyllide reduction [<xref ref-type="bibr" rid="CR26">26</xref>]. Pattanayak and Tripathy showed that over-expression of <italic>PORC</italic> in <italic>Arabidopsis</italic> led to coordinated up-regulation of gene/protein expression of several Chl biosynthetic pathway enzymes, thus enhancing Chl synthesis, and that the <sup>1</sup>O<sub>2</sub>-mediated photo-oxidative damage in transgenic plants overexpressing <italic>PORC</italic> was minimal under high light stress [<xref ref-type="bibr" rid="CR27">27</xref>]. The observed lower transcript level of <italic>PORC</italic> (TDF #171_2) in B-toxic <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the results that B-toxicity decreased the concentration of Chl a + b in citrus leaves (Figure <xref rid="Fig3" ref-type="fig">3</xref>E).</p><p>Cytochrome P450s play a key role in biotic and abiotic stresses. Transgenic tobacco and potato plants expressing <italic>cytochrome P450</italic> with increased monooxygenase activity tolerated better oxidative stress after herbicide treatment [<xref ref-type="bibr" rid="CR28">28</xref>]. We found that B-toxicity increased the expression levels of genes encoding cytochrome P450 (TDF #5_1) and cytochrome P450 like protein (TDF #76-1) in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), which agrees with the previous report that some of the 49 cytochrome P450 genes in <italic>Arabidopsis</italic> were upregulated by biotic (i.e., <italic>Alternaria brassicicola</italic> and <italic>Alternaria alternata</italic>) and abiotic [i.e., drought, high salinity, low temperature, hormones, paraquat, rose bengal, UV stress (UV-C), mechanical wounding and heavy metal stress (CuSO<sub>4</sub>)] stresses [<xref ref-type="bibr" rid="CR29">29</xref>]. Thus, the up-regulation of <italic>cytochrome P450s</italic> in B-toxic <italic>C. grandis</italic> leaves might be an adaptive response. However, B-toxicity decreased the expression of <italic>cytochrome P450</italic> in <italic>Arabidopsis</italic> roots [<xref ref-type="bibr" rid="CR7">7</xref>].</p><p>Taken all together, we isolated eight up-regulated and eight down-regulated TDFs from B-toxic <italic>C. grandis</italic> leaves, and five up-regulated and nine down-regulated from B-toxic <italic>C. sinesnsis</italic> ones. Among these differentially expressed TDFs, only <italic>SBPase</italic> (TDF #249_3) and <italic>PORC</italic> (TDF #171_2) were similarly affected by B-toxicity in the two species (Table <xref rid="Tab2" ref-type="table">2</xref>). These results demonstrated that the transcript profiles in the two species were differentially altered under B-toxicity.</p></sec><sec id="Sec10"><title>Leaf lipid metabolism</title><p>Allene oxide synthase (AOS) and hydroperoxide lyase (HPL) branches of the oxylipin pathway, which are responsible for the production of jasmonates and aldehydes, respectively, participate in a range of stresses. Recently, Liu et al. showed that depletion of rice <italic>OsHPL3</italic> greatly stimulated the jasmonic acid-governed defense response [<xref ref-type="bibr" rid="CR30">30</xref>]. Therefore, the AOS pathway and jasmonate level might be up-regulated in the B-toxic <italic>C. sinensis</italic> leaves due to decreased expression of <italic>fatty acid HPL</italic> (TDF #10_1; Table <xref rid="Tab2" ref-type="table">2</xref>), thus contributing to B-tolerance. In addition, B-toxicity also affected the transcript levels of three genes [i.e., <italic>plastidial pyruvate kinase 3</italic> (TDF #35_1), <italic>sugar</italic>-<italic>dependent1</italic> (TDF #195_1) and <italic>3</italic>-<italic>oxoacyl</italic>-<italic>reductase</italic> (TDF #233_3)] related to lipid metabolism in <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). Thus, lipid metabolism might be altered in B-toxic <italic>C. sinensis</italic> leaves.</p><p>Tang et al. reported that transgenic tobacco plants over-expressing <italic>acyl carrier protein</italic> (<italic>ACP</italic>)-<italic>1</italic> (or expressing antisense <italic>ACP1</italic>) exhibited an increase (or decrease) in leaf concentrations of total lipids and the main fatty acids, and were more tolerant (or sensitive) to cold stress [<xref ref-type="bibr" rid="CR31">31</xref>]. Branen et al. showed that reduction of <italic>ACP4</italic> by antisense RNA led to a decrease in total leaf lipids and decreased photosynthetic efficiency, and concluded that <italic>ACP4</italic> might play a major role in the biosynthesis of fatty acids for chloroplast membrane development [<xref ref-type="bibr" rid="CR32">32</xref>]. The lower transcript level of gene encoding ACP1, chloroplastic-like (TDF #8_1) in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) means that fatty acid biosynthesis in these leaves might be impaired. However, the expression of α/β-hydrolase domain-containing protein (TDF #194_1) and phospholipase-like protein (PEARLI 4) domain-containing protein (TDF #186_4) genes were up-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>).</p></sec><sec id="Sec11"><title>Leaf nucleic acid metabolism</title><p>As shown in Table <xref rid="Tab2" ref-type="table">2</xref>, eight up-regulated genes (TDFs #52_1, 49_1, 72_4, 120_1, 44_1, 159_2, 164_1 and 73_2) and nine down-regulated genes (TDFs #250_3, 157_2, 11_1, 71_3, 67_4, 10_4, 22_3, 104_1 and 68_2) were isolated from B-toxic <italic>C. grandis</italic> leaves, while only five up-regulated genes (TDFs #73_2, 250_3, 157_2, 60_1 and 131_1) and four down-regulated genes (TDFs #164_1, 71_3, 186_1 and 108_1) were identified in B-toxic <italic>C. sinensis</italic> leaves. Obviously, B-toxicity affected nucleic acid metabolism more in <italic>C. grandis</italic> leaves than in <italic>C. sinensis</italic> ones. This agrees with our inference that <italic>C. sinensis</italic> may tolerate higher level of B.</p></sec><sec id="Sec12"><title>Leaf protein and amino acid metabolism</title><p>All these differentially expressed TDFs encoding chloroplatic translation initiation factor IF-2 (TDF #236_1) involved in promoting the binding of formylmethionyl-tRNA to 30 S ribosomal subunits, eukaryotic release factor 1–3 (TDF #117_4) involved in the termination step of protein synthesis, EMB1241 (At5g17710; TDF #93_3 ) related to protein folding and stabilization, Ankyrin repeat domain-containing protein (TDF #73_3) involved mainly in mediating protein-protein interactions, and ribosomal proteins [i.e., 50S ribosomal protein L15 (TDF #179_4), 30S ribosomal protein S17 (TDF #105_1), putative 60S ribosomal protein L6 (TDF #99_6) and 60S ribosomal protein L4_1 (TDF #186_2) ] related to mature ribosome assembly and translation processes except for SHEPHERD (TDF #93_2) involved in the correct folding and/or complex formation of CLAVATA (CLV) proteins [<xref ref-type="bibr" rid="CR33">33</xref>], 60S ribosomal protein L23 (TDF #129_2) and 60S ribosomal protein L10B (TDF #161_1), were down-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), indicating that B-toxicity impairs protein biosynthesis in <italic>C. grandis</italic> leaves [<xref ref-type="bibr" rid="CR34">34</xref>,<xref ref-type="bibr" rid="CR35">35</xref>]. By contrast, only three down-regulated genes [30S ribosomal protein S17 (TDF #105_1), chaperonin 20 (TDF #98_1) involved in protein folding and stabilization and AT5G47880 (TDF #69_3) involved in the termination step of protein synthesis] were detected in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). These results demonstrated that B-toxicity affected protein biosynthesis more in the former than in the latter. This agrees with our data that B-toxicity only decreased total soluble protein concentration in <italic>C. grandis</italic> leaves (Figure <xref rid="Fig3" ref-type="fig">3</xref>H).</p><p>Here we observed four down-regulated genes [i.e., mitogen-activated protein (MAP) kinase (TDF #23_4), putative leucine-rich repeat receptor-like protein kinase (TDF #139-4), CBL-interacting protein kinase 19 (TDF #72_1) and At1g25390/F2J7_14 (TDF #39_3)] and three up-regulated genes [i.e., CDK activating kinase (TDF #12_2), serine/threonine protein kinase ATR (TDF #22_2) and receptor-like protein kinase (TDF #235_3) ] involved in phosphorylation and one up-regulated gene [i.e., protein phosphatase 2C (TDF #99_1)] involved in dephosphorylation in B-toxic <italic>C. grandis</italic> leaves, while only one down-regulated gene [i.e., receptor-like protein kinase (TDF #110_1)] and one up-regulated gene [i.e., protein phosphatase 2C (TDF #99_1)] in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). This means that <italic>C. sinensis</italic> leaves might achieve a better balance between phosphorylation and dephosphorylation than <italic>C. grandis</italic> ones under B-toxicity, which might contribute to the B-tolerance of <italic>C. sinensis</italic>.</p><p>Inactive (i.e., incorrect folding) and futile proteins for cell are tagged by ubiquitin for proteolysis [<xref ref-type="bibr" rid="CR36">36</xref>]. In this study, we found four up-regulated genes [i.e., C3H4 type zinc finger protein (TDF #99_2), AT5g57360/MSF19_2 (TDF #54_1), E3 ligase SAP5 (TDF #57_1) and root phototropism protein 2 (TDF #234_1)] and three down-regulated genes [i.e., E3 ubiquitin-protein ligase BRE1-like protein (TDF #96_1), Skp1-like protein 1 (TDF #187_1) and polyubiquitin (TDF #120_2)] involved in ubiquitination in B-toxic <italic>C. grandis</italic> leaves, and one up-regulated gene [i.e., putative E3 ubiquitin-protein ligase XBAT31 isoform 2 (TDF #158_2)] and two down-regulated genes [i.e., F-box family protein (TDF #73_1) and F-box with WD-40 2 (TDF #112_1)] involved in ubiquitination in B-toxici <italic>C. sinensis</italic> leaves. This indicates that ubiquitination might be involved in the adaptive response of citrus leaves to B-toxicity. Plant proteases has been shown to play key roles in controlling strict protein quality and degrading specific sets of proteins in response to environmental stresses [<xref ref-type="bibr" rid="CR37">37</xref>]. As expected, several genes (TDFs #38_3, 81_1, 38_4, 73_4, 240_1, 39_1, 145_1, 67_1 and 75_1) involved in proteolysis were altered in B-toxic <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>S-adenosylmethionine (AdoMet) participates in a number of essential metabolic pathways in plants and is the principal biological methyl donor. AdoMet-dependent methylation is essential for keeping cellular functions in plants [<xref ref-type="bibr" rid="CR38">38</xref>]. Methionine synthase, which catalyzes the last reaction in <italic>de novo</italic> methionine synthesis, also serves to regenerate the methyl group of AdoMet. As shown in Table <xref rid="Tab2" ref-type="table">2</xref>, B-toxicity increased the expression of AT4G01850 (TDF #138_4) involved in AdoMet biosynthesis in <italic>C. sinensis</italic> leaves, but decreased <italic>Methionine synthase</italic> expression (TDF #245_1) in <italic>C. grandis</italic> leaves, which might contribute to the higher tolerance of <italic>C. sinensis</italic> leaves to B-toxicity than that of <italic>C. grandis</italic> ones.</p><p>N-carbamoylputrescine amidase (TDF #213_4) involved in polyamine (putrescine) biosynthesis were down-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). This means that the biosynthesis of polyamine might be inhibited in B-toxic <italic>C. grandis</italic> leaves, which disagrees with the previous report that 1000 μM B increased leaf concentration of putrescine in B-sensitive barley cultivar, but decreased its concentration in B-tolerant one [<xref ref-type="bibr" rid="CR39">39</xref>].</p><p>The up-regulation of 2-oxoglutarate-dependent dioxygenase gene (TDF #61_2) in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the reports that B-toxicity stimulated the general amino acid control system in <italic>Saccharomyces cerevisiae</italic> [<xref ref-type="bibr" rid="CR35">35</xref>] and that the concentration of total amino acids in tomato leaves increased under B-toxicity [<xref ref-type="bibr" rid="CR40">40</xref>]. Evidence shows that 2-oxoglutarate-dependent dioxygenase participates in glucosinolate biosynthesis [<xref ref-type="bibr" rid="CR41">41</xref>]. Thus, the concentration of glucosinolates might be enhanced in B-toxic <italic>C. grandis</italic> leaves.</p><p>There is evidence showing that a few cystathionine-β-synthase (CBS) domain-containing proteins (CDCPs) play a role in plant stress response/tolerance and development [<xref ref-type="bibr" rid="CR42">42</xref>]. Overexpression of <italic>OsCBSX4</italic> improved tobacco plant tolerance to salinity, oxidative, and heavy metal stresses [<xref ref-type="bibr" rid="CR43">43</xref>]. We observed that B-toxicity decreased the transcript level of <italic>CDCP</italic> (TDF #251_3) in <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), as obtained on manganese (Mn)-toxic <italic>C. grandis</italic> leaves [<xref ref-type="bibr" rid="CR44">44</xref>]. However, B-deficient <italic>C. sinensis</italic> roots had higher level of CBS family protein [<xref ref-type="bibr" rid="CR45">45</xref>]. Singh et al. observed that the expression of <italic>OsCBSX4</italic> was up-regulated under high salinity, heavy metal, and oxidative stresses at seedling stage of a salt tolerant (Pokkali) rice cultivar, whilst its expression was upregulated only under NaCl stress, downregulated under heavy metal stress and kept unchanged under oxidative stress in a salt sensitive (IR64) rice one [<xref ref-type="bibr" rid="CR43">43</xref>]. Taken all together, the influence of stresses on expression of CDCP genes deponds on the kinds of stresses and plant species/cultivars.</p></sec><sec id="Sec13"><title>Leaf stress responses</title><p>Inorganic pyrophosphatase (PPase), which cleaves pyrophosphate molecules to liberate two molecules of inorganic phosphate, are essential for the viability of organisms, because the removal of pyrophosphate, a by-product of a host of biosynthetic reactions, is required for preventing the inhibition of thermodynamically unfavorable reactions [<xref ref-type="bibr" rid="CR46">46</xref>,<xref ref-type="bibr" rid="CR47">47</xref>]. George et al. observed that <italic>Nicotiana benthamiana</italic> plants lacking plastidial soluble PPase exhibited reduced drought tolerance as a result of the impaired leaf anabolic pathways [<xref ref-type="bibr" rid="CR46">46</xref>]. The up-regulation of <italic>PPase 1</italic> (TDF #118_1) in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) might be an adaptive response to B-toxicity. By contrast, its expression (TDF #118_1) was down-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>Because leaf CO<sub>2</sub> assimilation was decreased in B-toxic leaves (Figure <xref rid="Fig3" ref-type="fig">3</xref>A), less of the absorbed light energy was utilized in photosynthetic electron transport in these leaves, particularly under high light. Thus, reactive oxygen species (ROS) production might be enhanced in B-toxic leaves because of more excess absorbed photon flux [<xref ref-type="bibr" rid="CR14">14</xref>]. In addition to various ROS scavenger enzymes, “house-keeping” enzymes such as Nudix hydrolases (NUDXs) also play a role in ROS scavenging. Ogawa et al. [<xref ref-type="bibr" rid="CR48">48</xref>] and Ishikawa et al. [<xref ref-type="bibr" rid="CR49">49</xref>] showed that transgenic <italic>Arabidopsis</italic> plants overexpressing <italic>AtNUDX2</italic> and <italic>AtNUDX7</italic> exhibited higher tolerance to oxidative stress than wild type plants. Therefore, the higher expression level of <italic>NUDX19</italic> (TDF #148_2) in B-toxic <italic>C. sinensis</italic> leaves might be an adaptive response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>). However, its expression level (TDF #148_2) in <italic>C. grandis</italic> leaves decreased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>Up to 10% of the ascorbate content of the whole leaf is localized in the apoplast, where it forms the first line of defense against external oxidants [<xref ref-type="bibr" rid="CR50">50</xref>]. In the apoplast, ascorbate oxidase (AO) oxidizes ascorbate to the unstable radical monodehydroascorbate which rapidly disproportionates to yield dehydroascorbate and ascorbate, thus participating in the regulation of the redox state of ascorbic acid pool. AO has been suggested to play a role in cell expansion <italic>via</italic> the modulation of redox control of the apoplast [<xref ref-type="bibr" rid="CR51">51</xref>]. Pignocchi et al. [<xref ref-type="bibr" rid="CR52">52</xref>] showed that enhanced AO activity decreased the concentration and the redox state of ascorbic acid pool in the apoplast, whereas reduced AO activity increased its amount and redox state in the apoplast. Overexpression of <italic>AO</italic> in the apoplast of tobacco resulted in lowered capacity for scavenging ROS in the leaf apoplast accompanied by increased sensitivity to ozone [<xref ref-type="bibr" rid="CR53">53</xref>]. Fotopoulos et al. [<xref ref-type="bibr" rid="CR50">50</xref>] observed that <italic>AO</italic>-overexpressing transgenic tobacco plants had increased sensitivity to various oxidative stress-promoting agents accompanied by a general suppression of the plant antioxidative metabolism. By contrast, a diminution in AO activity improved tomato yield under water deficit [<xref ref-type="bibr" rid="CR54">54</xref>]. The down-regulation of gene encoding Fe (II)/ascorbate oxidase family protein SRG1 (TDF #59_1) in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) might increase the amount and the redox state of AA pool in the apoplast, thus enhancing the B-tolerance.</p><p>Thioredoxins, which participates in supplying reducing power to reductases required for detoxifying lipid hydroperoxides or repairing oxidized proteins, play key roles in plant tolerance of oxidative stress [<xref ref-type="bibr" rid="CR55">55</xref>]. We found that the expression level of <italic>thioredoxin superfamily protein</italic> (TDF #137_2) was up-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), indicating that thioredoxins might be involved in the ROS detoxification. However, the transcript level of thioredoxin superfamily protein (TDF #68_3) gene was down-regulated in B-toxic <italic>C. grandis</italic> leaves.</p><p>Our finding that B-toxicity increased the expression level of <italic>group 5 late embryogenesis abundant protein</italic> (LEA5, TDF #2_1) in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the previous report that drought, heat and salt stresses stimulated the expression of LEA5 in citrus leaves [<xref ref-type="bibr" rid="CR56">56</xref>]. Accumulation of AtRAB28 (LEA5) protein in <italic>Arabidopsis</italic> through transgenic approach improved the germination rate under standard conditions or salt and osmotic stresses and the cation toxicity tolerance [<xref ref-type="bibr" rid="CR57">57</xref>]. Also, B-toxicity increased the transcript level of <italic>thaumatin</italic>-<italic>like protein 1</italic> (TLP1, TDF #125_1) in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). The family of thaumatin-like proteins (also designated PR-5), which comprises proteins with various functions, is induced by biotic and abiotic factors in plants [<xref ref-type="bibr" rid="CR58">58</xref>]. Therefore, the up-regulation of <italic>LEA5</italic> and <italic>TLP1</italic> in B-toxic <italic>C. grandis</italic> leaves might be an adaptive response.</p><p>Protein sodium-and lithium-tolerant 1 (SLT1) gene isolated from tobacco (<italic>NtSLT1</italic>) and <italic>A. thaliana</italic> (<italic>AtSLT1</italic>) has been implicated in mediating salt tolerance by regulating Na<sup>+</sup> homeostasis <italic>via</italic> the calcineurin (CaN) and SPK1/HAL4 (SPK1/HAL4 which encodes a serine-threonine kinase) signal transduction [<xref ref-type="bibr" rid="CR59">59</xref>]. Later, Antoine et al. [<xref ref-type="bibr" rid="CR60">60</xref>] showed that rice <italic>OsSLT1</italic> had molecular chaperone activity <italic>in vitro</italic>, and that <italic>OsSLT1</italic> could be an important component of the cell immediate defenses against possible protein denaturation and aggregation. The down-regulation of <italic>SLT1</italic> (TDF #99_5) in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) means that Na<sup>+</sup> homeostasis or related processes mediated by <italic>SLT1</italic> are impaired in B-toxic <italic>C. grandis</italic> leaves.</p><p>Plant autophagy plays a role in various stress responses, pathogen defense, and senescence [<xref ref-type="bibr" rid="CR61">61</xref>]. Xiong et al. [<xref ref-type="bibr" rid="CR62">62</xref>,<xref ref-type="bibr" rid="CR63">63</xref>] showed that AtATG18a was necessary for the formation of autophagosomes during nutrient stress and senescence in <italic>A. thaliana</italic> and that autophagy participated in the degradation of oxidized proteins under oxidative stress conditions in <italic>Arabidopsis. AtATG18a</italic> RNAi plants usually senesce earlier and have lower tolerance to various stresses including drought, salt and oxidative stresses compared with wild-type plants [<xref ref-type="bibr" rid="CR61">61</xref>,<xref ref-type="bibr" rid="CR63">63</xref>]. Our result showed that the transcript level of <italic>transducin</italic>/<italic>WD40 domain</italic>-<italic>containing protein</italic> (ATG18a, TDF #104_3) in <italic>C. sinensis</italic> leaves decreased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>), indicating that autophagy is impaired in <italic>C. sinensis</italic> leaves.</p><p>As shown in Table <xref rid="Tab2" ref-type="table">2</xref>, B-toxicity down-regulated the expression of “cold-regulated” gene (cold regulated 314 thylakoid membrane 2, TDF # 109_1) in <italic>C. sinensis</italic> leaves and universal stress protein A-like protein (TDF #150_2) in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), indicating that B-toxicity might affect the tolerance of plants to other stresses.</p></sec><sec id="Sec14"><title>Leaf signal transduction</title><p>Here four genes involved in signal transduction were altered by B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref> and Figure <xref rid="Fig4" ref-type="fig">4</xref>). Evidence shows that that signal recognition particle 54 kDa protein (SRP54) plays important roles in chloroplast development [<xref ref-type="bibr" rid="CR64">64</xref>,<xref ref-type="bibr" rid="CR65">65</xref>]. The down-regulation of signal recognition particle 54 kDa protein 2 (TDF #182_2) in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) means that the biosynthesis of Chl is impaired in these leaves. This agrees with our results that B-toxicity affected Chl more in <italic>C. grandis</italic> leaves than in <italic>C. sinensis</italic> ones (Figure <xref rid="Fig3" ref-type="fig">3</xref>E).</p><p>Increasing evidence shows that 14-3-3 proteins play an important role in plant stress responses [<xref ref-type="bibr" rid="CR66">66</xref>,<xref ref-type="bibr" rid="CR67">67</xref>]. The most direct evidence for the role of 14-3-3 proteins in stress responses comes from transgenic rice plants over-expressing <italic>ZmGF14</italic>-<italic>6</italic> encoding a maize 14-3-3 protein [<xref ref-type="bibr" rid="CR68">68</xref>] and cotton plants over-expressing <italic>Arabidopsis</italic> 14-3-3λ [<xref ref-type="bibr" rid="CR69">69</xref>]. These transgenic plants displayed enhanced tolerance to drought stress. Heterotrimeric GTP-binding proteins (G proteins, consisting of subunits G<sub>α</sub>, G<sub>β</sub>, and G<sub>γ</sub>) are signaling molecules required for various eukaryotic organisms. Joo et al. [<xref ref-type="bibr" rid="CR70">70</xref>] observed that <italic>A. thaliana</italic> mutant plants losing the G<sub>β</sub> protein were less tolerant to O<sub>3</sub> damage than wild-type plants. Thus, the B-tolerance of <italic>C. grandis</italic> leaves might be down-regulated due to decreased transcript level of genes encoding 14-3-3 protein (TDF #108_2) and heterotrimeric GTP-binding protein subunit beta 1 (TDF #200_1) (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>In higher plants, the endogenous circadian clock is involved in the manipulation of different various cellular processes ranging from photosynthesis to stress responses [<xref ref-type="bibr" rid="CR71">71</xref>,<xref ref-type="bibr" rid="CR72">72</xref>]. It also confers plants with competitive advantages, including improved photosynthesis, growth and survival [<xref ref-type="bibr" rid="CR71">71</xref>]. Nakamichi et al. [<xref ref-type="bibr" rid="CR72">72</xref>] observed that A <italic>PRR9</italic>, <italic>7</italic> and <italic>5</italic> triple mutant of <italic>Arabidopsis</italic> had higher tolerance against drought, salt and cold stresses compared to wild type, demonstrating the involvement of the three genes in abiotic stress responses as negative regulators. The up-regulation of <italic>pseudo</italic>-<italic>response regulator</italic> 5 (<italic>PRR5</italic>; TDF #70_2) in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the previous reports that <italic>PRR5</italic> was induced by cold treatment in apical shoots of cassava [<xref ref-type="bibr" rid="CR73">73</xref>] and in <italic>Arabidopsis</italic> leaves [<xref ref-type="bibr" rid="CR74">74</xref>]. Fukushima et al. [<xref ref-type="bibr" rid="CR75">75</xref>] showed that PRR9, 7 and 5 negatively regulated the biosynthetic pathways of Chl, Car, ABA and α-tocopherol. This agrees with our results that B-toxici <italic>C. sinensis</italic> leaves had decreased concentrations of Chl a + b and Car (Figure <xref rid="Fig3" ref-type="fig">3</xref>E and H).</p></sec><sec id="Sec15"><title>Leaf cell transport</title><p>As shown in Table <xref rid="Tab2" ref-type="table">2</xref> and Figure <xref rid="Fig4" ref-type="fig">4</xref>, the number of differentially expressed TDFs involved in cell transport was far less in B-toxic <italic>C. sinensis</italic> leaves than in B-toxic <italic>C. grandis</italic> ones, meaning that cell transport is less affected in the former than in the latter, which agrees with our inference that <italic>C. sinensis</italic> leaves may tolerate higher level of B.</p><p>Most of the differentially expressed TDFs (TDFs #26_1, 124_3, 66_1, 97_1, 53_1, 210_1, 178_1, 49_3, 137_1, 63_1, 51_1, 250_2, 79_2 and 67_3) associated with cell transport were up-regulated in B-toxic <italic>C. grandis</italic> leaves except for AT5g24810/F6A4_20 (TDF #89_2), protein transport protein SEC61 γ subunit (TDF #6_1) and putative β-subunit of adaptor protein complex 3, PAT2 (TDF #249_2) (Table <xref rid="Tab2" ref-type="table">2</xref>), indicating that cell transport might be enhanced in B-toxic <italic>C. grandis</italic> leaves. Plasma-membrane H<sup>+</sup>-ATPase plays a crucial role in the plant response to environmental stresses, such as salt stress, aluminum (Al) stress, P and potassium (K) deficiencies [<xref ref-type="bibr" rid="CR76">76</xref>]. Wu et al. [<xref ref-type="bibr" rid="CR77">77</xref>] reported that pumping of Ca<sup>2+</sup> and Mn<sup>2+</sup> by an endoplasmic reticulum-type Ca<sup>2+</sup>-ATPase (ECA1) into the endoplasmic reticulum was necessary for maintaining plant growth under calcium (Ca)-deficiency or Mn-toxicity. The P<sub>IB</sub>-ATPases (also known as heavy metal ATPases), which are involved in heavy metal transport across cellular membranes, play a crucial role in metal homeostasis and detoxification in plants [<xref ref-type="bibr" rid="CR78">78</xref>]. Proton pump interactor 1 (PPI1), an interactor of plasma-membrane H<sup>+</sup>-ATPase, stimulates its activity <italic>in vitro</italic> [<xref ref-type="bibr" rid="CR79">79</xref>]. The up-regulation of <italic>PPI1</italic> (TDF #97_1) in B-toxic leaves agrees with our data that the transcript level of <italic>H</italic><sup>+</sup>-<italic>ATPase 6</italic> (TDF #26_1) in <italic>C. grandis</italic> leaves increased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>) and with the report that the expression of <italic>PPI1</italic> in potato tuber was up-regulated by salt stress and cold [<xref ref-type="bibr" rid="CR79">79</xref>].</p><p>ATP-binding cassette (ABC) transporters are involved in metal ion efflux from the plasma-membrane. AtPDR8, an ABC transporter localized in the plasma-membrane of <italic>A. thaliana</italic> root hairs and epidermal cells, confers metal tolerance [<xref ref-type="bibr" rid="CR80">80</xref>]. Our finding that the expression of ABC transporter G family member 40 (TDF #53_1) gene was up-regulated in B-toxic <italic>C. grandis</italic> leaves agrees with the reports that <italic>AtPDR8</italic> in <italic>Arabidopsis</italic> roots and shoots was induced when exposed to copper (Cu), cadmium (Cd) and lead (Pb) [<xref ref-type="bibr" rid="CR80">80</xref>], and that ABC transporter G family member 40 gene and ABC transporter A family member 7 gene were induced in drought-sensitive and -tolerant genotypes of <italic>Gossypium herbaceum</italic>, respectively under drought stress [<xref ref-type="bibr" rid="CR81">81</xref>]. However, the expression of AT5g24810/F6A4_20 (TDF #89_2) was down-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>Cu transporters (COPTs/Ctrs) are involved in the maintenance of Cu homeostasis in plants. Generally speaking, <italic>COPTs</italic>/<italic>Ctrs</italic> are up-regulated by Cu deprivation and down-regulated by Cu excess [<xref ref-type="bibr" rid="CR82">82</xref>]. <italic>COPT1</italic> antisense <italic>Arabidopsis</italic> plants have decreased Cu level due to decreased Cu uptake and display sensitivity to Cu chelators [<xref ref-type="bibr" rid="CR83">83</xref>]. The up-regulation of COPT (TDF #210_1) in B-toxic <italic>C. grandis</italic> leaves might play a role in the maintenance of leaf Cu homeostasis.</p><p>Plant cyclic nucleotide gated channels (CNGCs) paly a role in heavy metal homeostasis. Previous study showed that transgenic tobacco plants overexpressing a truncated <italic>NtCBP4</italic> (tobacco <italic>CNGC</italic>) had higher tolerance to Pb compared with wild type [<xref ref-type="bibr" rid="CR84">84</xref>]. Chan et al. [<xref ref-type="bibr" rid="CR85">85</xref>] reported that <italic>cngc2 Arabidopsis</italic> mutants were hypersensitive to increased soil Ca. However, transgenic tobacco plants overexpressing <italic>NtCBP</italic>4 were hypersensitivity to Pb [<xref ref-type="bibr" rid="CR86">86</xref>]. B-toxicity-induced increase in transcript level of <italic>CNGC1</italic> (TDF #178_1) in <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the report that the expression of <italic>AtCNGC2</italic> was induced during <italic>Arabidopsis</italic> leaf senescence and <italic>AtCNGC2</italic> might be involved in programmed cell death [<xref ref-type="bibr" rid="CR87">87</xref>].</p><p>Membrane traffic is not only required for plant normal cellular function and maintenance of cellular viability, but also plays an important roles in plant responses to the environment [<xref ref-type="bibr" rid="CR88">88</xref>,<xref ref-type="bibr" rid="CR89">89</xref>]. The transcript levels of genes [i.e., vacuolar-sorting receptor 3 (TDF #49_3), vacuolar protein-sorting-associated protein 37–1 (TDF #137_1), vesicle-associated membrane protein-associated protein (TDF #63_1), secY protein transport family protein (TDF #51-1), fat-free-like protein (TDF #250_2) and non-specific lipid-transfer protein (TDF #79_2)] involved in membrane traffic increased in B-toxic <italic>C. grandis</italic> leaves except for genes encoding protein transport protein SEC61 γ subunit (TDF #6_1) and putative β-subunit of adaptor protein complex 3, PAT2 (TDF # 249_2) (Table <xref rid="Tab2" ref-type="table">2</xref>). This indicates that membrane traffic might be enhanced in B-toxic <italic>C. grandis</italic> leaves.</p><p>Plant sieve element occlusion (SEO) genes have been shown to encode the common phloem proteins (P-proteins) that plug sieve plates after wounding. Tobacco <italic>SEO</italic>-RNA interference lines were essentially devoid of P-protein structures and lost photoassimilates more rapidly after injury than control plants [<xref ref-type="bibr" rid="CR90">90</xref>]. Therefore, the up-regulation of sieve element occlusion protein 1 gene (TDF #67_3) in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) might be of advantage to prevent the loss of photoassimilates. Recently, Huang et al. observed that many electron-dense particles deposited near sieve plates of B-toxic <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves [<xref ref-type="bibr" rid="CR13">13</xref>]. In conclusion, the up-regulation of cell transport in B-toxic <italic>C. grandis</italic> leaves might be an adaptive response of plants to B-toxicity.</p><p>By contrast, we isolated three down-regulated [i.e., putative β-subunit of adaptor protein complex 3, PAT2 (TDF #249_2), sugar transporter ERD6-like 5 (TDF #61_1) and metal tolerance protein (MTP, TDF #179_2)] and three up-regulated [i.e., sieve element occlusion protein 1 (TDF #67_3), kinesin-related protein (TDF #51_4) and bidirectional sugar transporter SWEET7 (TDF #36_2) TDFs from B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). Generally speaking, cell transport might be not enhanced in B-toxicity leaves.</p><p>In plants, kinesins are involved in a variety of cellular processes including intracellular transport, spindle assembly, phragmoplast assembly, chromosome motility, MAP kinase regulation and microtubule stability [<xref ref-type="bibr" rid="CR91">91</xref>]. Li et al. [<xref ref-type="bibr" rid="CR92">92</xref>] reported that mutation of rice <italic>BC12</italic>/<italic>GDD1</italic> encoding a kinesin-like protein led to dwarfism with impaired cell elongation. Nishihama et al. [<xref ref-type="bibr" rid="CR93">93</xref>] demonstrated that the expansion of the cell plate in tobacco plant cytokinesis required kinesin-like proteins (i.e., NACK1 and NACK2) to regulate the activity and localization of MAP kinase kinase kinase. Therefore, the up-regulation of <italic>kinesin</italic>-<italic>like protein</italic> (TDF #51_4) in <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) might be an adaptive responsive to B-toxicity. However, the transcript level of putative β-subunit of adaptor protein complex 3, PAT2 (TDF #249_2) in <italic>C. sinensis</italic> leaves decreased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>Plant SWEETs function as facilitators involved in the influx and the efflux of sugar into and out of cells [<xref ref-type="bibr" rid="CR94">94</xref>]. We found that the expression level of <italic>SWEET7</italic> (TDF #36_2) in <italic>C. sinensis</italic> leaves increased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>), which agrees with the previous report that <italic>SWEET15</italic>/<italic>SAG29</italic> was enhanced in senescing <italic>Arabidopsis</italic> leaves [<xref ref-type="bibr" rid="CR95">95</xref>]. However, the expression of gene encoding sugar transporter ERD6-like 5 (TDF #61_1), a passive facilitator for the diffusion of glucose across the tonoplast membrane, was down-regulated in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>). This disagrees with the previous report that the expression of <italic>AtESL1</italic> (<italic>ERD six</italic>-<italic>like 1</italic>) was induced by various stresses including drought, high salinity and ABA in <italic>Arabidopsis</italic> plants [<xref ref-type="bibr" rid="CR96">96</xref>].</p><p>MTPs are a subfamily of the cation diffusion facilitator (CDF) family found in plants. So far, most studied CDF family members confer heavy metal tolerance by affecting heavy metal efflux from the cytoplasm [<xref ref-type="bibr" rid="CR97">97</xref>]. The down-regulation of <italic>MTP</italic> (TDF #179_2) in <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) means that the tolerance of plants to heavy metal might be reduced in B-toxic plants. This agrees with our previous report that the tolerance of <italic>C. grandis</italic> plants to Al-toxicity was higher under adequate B supply than under excess B [<xref ref-type="bibr" rid="CR98">98</xref>].</p></sec><sec id="Sec16"><title>Leaf cell wall and cytoskeleton modification</title><p>Eleven TDFs associated with cell wall and cytoskeleton modification were altered by B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref> and Figure <xref rid="Fig4" ref-type="fig">4</xref>). O-methyltransferase (OMT) genes are involved in lignin biosynthesis. Fu et al. [<xref ref-type="bibr" rid="CR99">99</xref>] showed that down-regulation of the caffeic acid 3-O-methyltransferase (COMT) gene in switchgrass lowered lignin level in whole tillers and stems of transgenic plants and enhanced forage quality. Transgenic <italic>Leucaena leucocephala</italic> plants expressing antisense <italic>OMT</italic> displayed decreased activity of OMT activity and concentration of lignin [<xref ref-type="bibr" rid="CR100">100</xref>]. Therefore, the biosynthesis of lignin in B-toxic <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves might be reduced due to decreased expression of <italic>COMT</italic> (TDF #49_4) and <italic>COMT3</italic> (TDF #125_2) (Table <xref rid="Tab2" ref-type="table">2</xref>). In addition, the biosynthesis of chitin in <italic>C. grandis</italic> and <italic>C. sinensis</italic> leaves and cellulose in <italic>C. grandis</italic> leaves might be down-regulated under B-toxicity due to the down-regulation of <italic>chitinase</italic> (TDF #10_3) and c<italic>ellulose synthase</italic> (TDF #249_4) (Table <xref rid="Tab2" ref-type="table">2</xref>). These results demonstrated that B-toxicity might impair citrus cell wall metabolism, which agrees with the previous suggestion that leaf cupping, a specific visible B-toxic symptom in some species might be due to the inhibition of cell wall expansion, through disturbance of cell wall crosslinks [<xref ref-type="bibr" rid="CR101">101</xref>]. However, the transcript levels of genes encoding OMT1 (TDF #33_3), LIM domain-containing protein (TDF #241_1), UDP-glucose flavonoid 7-O-glucosyltransferase (TDF #124_2), UDP-glucosyltransferase family 1 protein (TDF #3_3), limonoid UDP-glucosyltransferase (TDF #70_4) and putative glucosyltransferase (TDF #63_2) in <italic>C. grandis</italic> increased in response to B-toxicity (Table <xref rid="Tab2" ref-type="table">2</xref>).</p><p>Evidence shows that lily LIM1 [<xref ref-type="bibr" rid="CR87">87</xref>] and all <italic>Arabidopsis</italic> LIM domain proteins [<xref ref-type="bibr" rid="CR102">102</xref>] participate in regulating actin cytoskeleton organization and dynamics. Tobacco LIM1 protein acts in the cytoplasm as an actin binding and bundling protein [<xref ref-type="bibr" rid="CR103">103</xref>] and in the nucleus as a transcription factor regulating the expression of genes related to lignin biosynthesis [<xref ref-type="bibr" rid="CR104">104</xref>]. Recently, Moes et al. [<xref ref-type="bibr" rid="CR105">105</xref>] demonstrated the involvement of tobacco LIM2 in actin-bundling and histone gene transcription. The up-regulation of <italic>LIM domain</italic>-<italic>containing protein</italic> (TDF #241_1) in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the report that the expression of <italic>LIM domain</italic>-<italic>containing protein</italic> in <italic>Physcomitrella patens</italic> increased under cold acclimation [<xref ref-type="bibr" rid="CR106">106</xref>].</p><p>Glycosyltransferases (GTs), which catalyze the formation of glycosidic bonds between donor sugars and acceptor molecules, participate in many aspects of a plant life, including cell wall biosynthesis [<xref ref-type="bibr" rid="CR107">107</xref>,<xref ref-type="bibr" rid="CR108">108</xref>]. In <italic>Arabidopsis</italic>, up to 10 or 12 GT2 family members form the cellulose synthase catalytic subunit and callose synthase gene families [<xref ref-type="bibr" rid="CR108">108</xref>]. In plants, UDP-glucosyltransferases (UGTs) have been suggested to play important roles in keeping cell homeostasis, regulating plant growth and improving their tolerance to environmental stresses [<xref ref-type="bibr" rid="CR109">109</xref>]. Overexpression of <italic>UGT74E2</italic> conferred tolerance to salinity and drought stresses in <italic>A. thaliana</italic> [<xref ref-type="bibr" rid="CR110">110</xref>]. Transgenic tobacco plants overexpressiong <italic>UGT85A5</italic> exhibited enhanced salt tolerance [<xref ref-type="bibr" rid="CR111">111</xref>]. Therefore, the up-regulation of UDP-glucose flavonoid 7-O-glucosyltransferase (TDF #124_2), UGT family 1 protein (TDF #3_3), limonoid UGT (TDF #70_4) and putative GT (TDF #63_2) genes in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) might play a role in B-tolerance of plants. However, loss of function of a <italic>UGT73B2</italic> alone or in conjunction with <italic>UGT73B1</italic> and <italic>UGT73B3</italic> resulted in enhanced oxidative stress tolerance in <italic>Arabidopsis</italic>, whilst transgenic <italic>Arabidopsis</italic> plants overexpressing <italic>UGT73B2</italic> displayed decreased oxidative stress tolerance [<xref ref-type="bibr" rid="CR112">112</xref>].</p></sec><sec id="Sec17"><title>Others</title><p>Overexpression of bacterial or plant gene encoding phytoene synthase (PSY), a key regulatory enzyme in Car biosynthesis, led to enhanced level of total Car in various higher plants [<xref ref-type="bibr" rid="CR113">113</xref>,<xref ref-type="bibr" rid="CR114">114</xref>]. Transgenic <italic>Arabidopsis</italic> plants overexpressing <italic>PSY</italic> from euhalophyte <italic>Salicornia europaea</italic> had higher tolerance to salt stress than wild type plants by enhanced photosynthetic efficiency and antioxidative capacity [<xref ref-type="bibr" rid="CR115">115</xref>]. Cidade et al. [<xref ref-type="bibr" rid="CR116">116</xref>] showed that ectopic expression of <italic>PSY</italic> from <italic>Citrus paradisi</italic> fruit conferred abiotic stress tolerance in transgenic tobacco, which was correlated with the increased endogenous ABA level and expression of stress-responsive genes. Our finding that B-toxic <italic>C. grandis</italic> leaves had lower transcript of <italic>PSY</italic> (TDF #229_4; Table <xref rid="Tab2" ref-type="table">2</xref>) means that the biosynthesis of Car and the antioxidative capacity may be decreased in B-toxic leaves. This agrees with our data that B-toxicity affected Car more in <italic>C. grandis</italic> leaves than in <italic>C. sinensis</italic> one (Figure <xref rid="Fig3" ref-type="fig">3</xref>G) and the inference that <italic>C. grandis</italic> may tolerate lower level of B.</p><p>Strictosidine synthase (Str), a key enzyme in alkaloid biosynthesis, catalyzes the condensation of tryptamine and secologanin leading to the synthesis of numerous monoterpenoid indole alkaloids in higher plants [<xref ref-type="bibr" rid="CR117">117</xref>]. The up-regulation of Str family protein gene (TDF #231_1) in B-toxic <italic>C. sinensis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>) agrees with the previous report that <italic>Str</italic> in <italic>Catharanthus roseus</italic> leaves was enhanced under dehydration, salt and UV stresses [<xref ref-type="bibr" rid="CR117">117</xref>] and that B-toxicity decreased IAA level in <italic>Triticum durum</italic> seedlings [<xref ref-type="bibr" rid="CR118">118</xref>], because the expression of <italic>Str</italic> was inhibited by auxin [<xref ref-type="bibr" rid="CR119">119</xref>]. B-toxicity-induced up-regulation of Str family protein gene (TDF #231_1) also agrees with our reference that the AOS pathway and jasmonate level might be up-regulated in the B-toxic <italic>C. sinensis</italic> leaves due to decreased expression of fatty acid HPL gene (TDF #10_1) (Table <xref rid="Tab2" ref-type="table">2</xref>), because <italic>Str</italic> has been shown to be induced by jasmonate [<xref ref-type="bibr" rid="CR120">120</xref>]. By contrast, the expression of Str family protein gene (TDF #231_1) was down-regulated in B-toxic <italic>C. grandis</italic> leaves (Table <xref rid="Tab2" ref-type="table">2</xref>), which agrees with the previous report that cold stress led to <italic>Str</italic> down-regulation in <italic>C. roseus</italic> leaves [<xref ref-type="bibr" rid="CR117">117</xref>].</p></sec></sec><sec id="Sec18" sec-type="conclusion"><title>Conclusions</title><p>B-toxicity affected <italic>C. grandis</italic> seedling growth, leaf CO<sub>2</sub> assimilation, pigments, total soluble protein, MDA and P more than <italic>C. sinensis</italic>, indicating that <italic>C. sinensis</italic> have higher B-tolerance than <italic>C. grandis</italic> ones. Under B-toxicity, <italic>C. sinensis</italic> leaves accumulated more B than <italic>C. grandis</italic> ones, meaning that the former may tolerate higher level of B. Using cDNA-AFLP, we successfully isolated 67 up-regulated and 65 down-regulated TDFs from B-toxic <italic>C. grandis</italic> leaves, whilst only 31 up-regulated and 37 down-regulated TDFs from B-toxic <italic>C. sinensis</italic> ones. This indicates that gene expression is less affected in B-toxic <italic>C. sinensis</italic> leaves than in <italic>C. grandis</italic> ones, which might be associated with the fact that <italic>C. sinensis</italic> leaves can tolerate higher level of B. The higher B-tolerance of <italic>C. sinensis</italic> might be related to the findings that B-toxic <italic>C. sinensis</italic> leaves had higher expression levels of genes involved in photosynthesis, which might contribute to the higher photosynthesis and light utilization and less excess light energy compared to the B-toxic <italic>C. grandis</italic> ones, and in ROS scavenging, thus preventing them from photo-oxidative damage. In addition, B-toxicity-induced alteration in the expression levels of genes encoding inorganic PPase 1, AT4G01850 and methionine synthase differed between the two species, which might also contribute to the B-tolerance of <italic>C. sinensis</italic>. In this study, a total of 174 differentially expressed TDFs were isolated from two citrus species, only 26 TDFs presented in the two citrus, the remaining TDFs presented only in <italic>C. grandis</italic> or <italic>C. sinensis</italic>, demonstrating that the B-toxicity-responsive genes differ between the two citrus species. For example, cell transport were up-regulated in B-toxicity <italic>C. grandis</italic> leaves, whilst this did not occur in B-toxic <italic>C. sinensis</italic> ones.</p></sec><sec id="Sec19" sec-type="materials|methods"><title>Methods</title><sec id="Sec20"><title>Plant materials</title><p>This study was conducted from February to December, 2011 at Fujian Agriculture and Forestry University. Plant culture and B treatments were performed according to Han et al. [<xref ref-type="bibr" rid="CR14">14</xref>]. Briefly, 5-week-old uniform seedlings of ‘Xuegan’ (<italic>Citrus sinensis</italic>) and ‘Sour pummelo’ (<italic>Citrus grandis</italic>) were transplanted to 6 L pots containing fine river sand. Plants, two per pot, were grown in a greenhouse under natural photoperiod at Fujian Agriculture and Forestry University. Eight weeks after transplanting, each pot was supplied every other day until dripping with nutrient solution containing 10 μM (control) or 400 μM (B-toxic) H<sub>3</sub>BO<sub>3</sub> and 6 mM KNO<sub>3</sub>, 4 mM Ca (NO<sub>3</sub>)<sub>2</sub>, 2 mM NH<sub>4</sub>H<sub>2</sub>PO<sub>4</sub>, 1 mM MgSO<sub>4</sub>, 10 μM H<sub>3</sub>BO<sub>3</sub>, 2 μM MnCl<sub>2</sub>, 2 μM ZnSO<sub>4</sub>, 0.5 μM CuSO<sub>4</sub>, 0.065 μM (NH<sub>4</sub>)<sub>6</sub>Mo<sub>7</sub>O<sub>24</sub> and 20 μM Fe-EDTA for 15 weeks. At the end of the experiment, fully expanded leaves from different replicates and treatments were used for all the measurements. Leaves were collected at noon under full sun and immediately frozen in liquid nitrogen and were stored at −80°C until extraction.</p></sec><sec id="Sec21"><title>Measurements of plant DW, root and leaf B, leaf P, total soluble protein, MDA and pigments</title><p>Ten plants per treatment from different pots were harvested and divided into their parts (roots and shoots). The plant parts were then dried at 75°C for 48 h and their DWs measured. B concentration in roots and leaves was assayed by ICP emission spectrometry after microwave digestion with HNO<sub>3</sub> [<xref ref-type="bibr" rid="CR121">121</xref>]. Leaf P concentration was measured according to Ames [<xref ref-type="bibr" rid="CR122">122</xref>]. Leaf total soluble protein was measured according to Bradford [<xref ref-type="bibr" rid="CR123">123</xref>] using bovine serum albumin as standard after being extracted with 50 mM Na<sub>2</sub>HPO<sub>4</sub>-KH<sub>2</sub>PO<sub>4</sub> (pH 7.0) and 5% (w/v) insoluble polyvinylpyrrolidone. Extraction and determination of leaf MDA were performed according to Hodges et al. [<xref ref-type="bibr" rid="CR124">124</xref>]. Chl, Chl a, Chl b and Car were assayed according to Lichtenthaler [<xref ref-type="bibr" rid="CR125">125</xref>] after being extracted with 80 (v/v) actetone.</p></sec><sec id="Sec22"><title>Measurements of leaf gas exchange</title><p>Leaf gas exchange was measured using a CIARS-2 portable photosynthesis system (PP systems, Herts, UK) at ambient CO<sub>2</sub> concentration under a controlled light intensity of 990–1010 μmol m<sup>−2</sup> s<sup>−1</sup> between 9:00 and 11:00 on a clear day. During measuring, leaf temperature and air relative humidity were 32.2 ± 0.2°C and 66.6 ± 0.8%, respectively.</p></sec><sec id="Sec23"><title>Leaf RNA extraction, cDNA synthesis and cDNA-AFLP analysis</title><p>Total RNA was extracted from ca. 300 mg of frozen mixed leaves from B-toxic and control plants of <italic>C. grandis</italic> and <italic>C. sinensis</italic> using Recalcirtant Plant Total RNA Extraction Kit (Centrifugal column type, Bioteke Corporation, China). There were three biological replicates for each treatment. Leave of 4–5 plants from different pots were mixed as a biological replicate. Equal amounts of leaves were collected from each plant. cDNA synthesis and cDNA-AFLP analysis were performed according to Zhou et al. [<xref ref-type="bibr" rid="CR44">44</xref>].</p></sec><sec id="Sec24"><title>Validation of cDNA-AFLP data using qRT-PCR</title><p>Total RNA was extracted from the frozen leaves as described above. qRT-PCR analysis was performed according to Zhou et al. [<xref ref-type="bibr" rid="CR44">44</xref>]. Specific primers were designed from the sequences of 16 differentially expressed TDFs using Primer Primier Version 5.0 (PREMIER Biosoft International, CA, USA). The sequences of the F and R primers used were listed in Additional file <xref rid="MOESM3" ref-type="media">3</xref>. Samples for qRT-PCR were run in 3 biological replicates with 3 technical replicates. Leave of 4–5 plants from different pots were mixed as a biological replicate. Relative gene expression was calculated using ddCt algorithm. For the normalization of gene expression, citrus <italic>actin</italic> (GU911361.1) was used as an internal standard and the leaves from control plants were used as reference sample, which was set to 1.</p></sec><sec id="Sec25"><title>Experimental design and statistical analysis</title><p>There were 20 pots (40 seedlings) per treatment in a completely randomized design. Experiments were performed with 3–10 replicates. Results represented the mean ± SE. Statistical analyses of data were carried out by ANOVA tests. Means were separated by the least significant difference test at <italic>P</italic> <0.05 level.</p></sec></sec></body><back><app-group><app id="App1"><sec id="Sec26"><title>Additional files</title><p><media position="anchor" xlink:href="12870_2014_284_MOESM1_ESM.doc" id="MOESM1"><label>Additional file 1:</label><caption><p><bold>Boron (B)-toxic symptoms on</bold><bold><italic>Citrus grandis</italic></bold><bold>and</bold><bold><italic>Citrus sinensis</italic></bold><bold>leaves.</bold> 1: Control leaves of <italic>C. grandis</italic>; 2: B-toxic leaves of <italic>C. grandis</italic>; 3: Control leaves of <italic>C. sinensis</italic>; 4: B-toxic leaves of <italic>C. sinensis</italic>.</p></caption></media><media position="anchor" xlink:href="12870_2014_284_MOESM2_ESM.doc" id="MOESM2"><label>Additional file 2:</label><caption><p><bold>cDNA-AFLP profiles using one</bold><bold><italic>Eco</italic></bold><bold><italic>R I selective primer and eight</italic></bold><bold><italic>Mes</italic></bold><bold>I selective primers.</bold> One <italic>Eco</italic>R I selective primer: <italic>Eco</italic>R I-GC; Eight <italic>Mes</italic> I selective primers: <italic>Mes</italic> I-GT, GA, TC, TG, TT, TA, AC and AG). 1: Control leaves of <italic>Citrus grandis</italic>; 2: B-toxicity leaves of <italic>C. grandis</italic>; 3: Control leaves of <italic>Citrus sinensis</italic>; 4: B-toxicity leaves of <italic>C. sinenis</italic>. Arrows indicate differentially expressed TDFs.</p></caption></media><media position="anchor" xlink:href="12870_2014_284_MOESM3_ESM.doc" id="MOESM3"><label>Additional file 3:</label><caption><p><bold>Specific primer pairs used for qRT-PCR expression analysis.</bold></p></caption></media></p></sec></app></app-group><glossary><title>Abbreviations</title><def-list><def-item><term>ABC</term><def><p>ATP-binding cassette</p></def></def-item><def-item><term>ACP</term><def><p>Acyl carrier protein</p></def></def-item><def-item><term>AdoMet</term><def><p>S-adenosylmethionine</p></def></def-item><def-item><term>AO</term><def><p>Ascorbate oxidase</p></def></def-item><def-item><term>AOS</term><def><p>Allene oxide synthase</p></def></def-item><def-item><term>B</term><def><p>Boron</p></def></def-item><def-item><term>Car</term><def><p>carotenoid</p></def></def-item><def-item><term>CBS</term><def><p>Cystathionine-β-synthase</p></def></def-item><def-item><term>CDCP</term><def><p>CBS domain-containing protein</p></def></def-item><def-item><term>CDF</term><def><p>Cation diffusion facilitator</p></def></def-item><def-item><term>cDNA-AFLP</term><def><p>cDNA-amplified fragment length polymorphism</p></def></def-item><def-item><term>Chl</term><def><p>Chlorophyll</p></def></def-item><def-item><term>CNGC</term><def><p>Cyclic nucleotide gated channel</p></def></def-item><def-item><term>COMT</term><def><p>Caffeic acid 3-O-methyltransferase</p></def></def-item><def-item><term>COPT</term><def><p>Cu transporters</p></def></def-item><def-item><term>DW</term><def><p>Dry weight</p></def></def-item><def-item><term>GT</term><def><p>Glycosyltransferase</p></def></def-item><def-item><term>HPL</term><def><p>Hydroperoxide lyase</p></def></def-item><def-item><term>IF</term><def><p>Initiation factor</p></def></def-item><def-item><term>LEA5</term><def><p>Group 5 late embryogenesis abundant protein</p></def></def-item><def-item><term>MAP</term><def><p>Mitogen-activated protein</p></def></def-item><def-item><term>MATE</term><def><p>Multi-drug and toxic compound extrusion</p></def></def-item><def-item><term>MDA</term><def><p>Malondialdehyde</p></def></def-item><def-item><term>MTP</term><def><p>Metal tolerance protein</p></def></def-item><def-item><term>NUDX</term><def><p>Nudix hydrolases</p></def></def-item><def-item><term>OMT</term><def><p>O-methyltransferase</p></def></def-item><def-item><term>POR</term><def><p>Protochlorophyllide oxidoreductase</p></def></def-item><def-item><term>PPase</term><def><p>Pyrophosphatase</p></def></def-item><def-item><term>PPI1</term><def><p>Proton pump interactor 1</p></def></def-item><def-item><term>PRR</term><def><p>Pseudo-response regulator 5</p></def></def-item><def-item><term>PsbA</term><def><p>PSII 32 kDa protein</p></def></def-item><def-item><term>PsbP</term><def><p>PSII 23 kDa protein</p></def></def-item><def-item><term>PSI</term><def><p>Photosystem I</p></def></def-item><def-item><term>PSII</term><def><p>Photosystem II</p></def></def-item><def-item><term>PSY</term><def><p>Phytoene synthase</p></def></def-item><def-item><term>RNAi</term><def><p>RNA interference</p></def></def-item><def-item><term>ROS</term><def><p>Reactive oxygen species</p></def></def-item><def-item><term>Rubisco</term><def><p>RuBP carboxylase/oxygenase</p></def></def-item><def-item><term>RuBP</term><def><p>ribulose-1,5-bisphosphate</p></def></def-item><def-item><term>SBPase</term><def><p>Sedoheptulose-1,7-bisphosphatase</p></def></def-item><def-item><term>SEO</term><def><p>Sieve element occlusion</p></def></def-item><def-item><term>SLT1</term><def><p>Protein sodium-and lithium-tolerant 1</p></def></def-item><def-item><term>Str</term><def><p>Strictosidine synthase</p></def></def-item><def-item><term>TDF</term><def><p>Transcript-derived fragments</p></def></def-item><def-item><term>TLP</term><def><p>Thaumatin-like protein</p></def></def-item><def-item><term>UGT</term><def><p>UDP-glucosyltransferase.</p></def></def-item></def-list></glossary><fn-group><fn><p><bold>Competing interests</bold></p><p>The authors declare that they have no competing interests.</p></fn><fn><p><bold>Authors’ contributions</bold></p><p>PG carried out most of the experiments and drafted the manuscript. YPQ participated in the design of the study. LTY participated in the design of the study and coordination. XY carried out the measurement of B and P. HXJ performed the statistical analysis. JHH carried out the cultivation of seedlings. LSC designed and directed the study and revised the manuscript. 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