Glutathione S-Transferase Gene Family in Gossypium raimondii and G. arboreum: Comparative Genomic Study and their Expression under Salt Stress
Identifieur interne : 000302 ( Pmc/Corpus ); précédent : 000301; suivant : 000303Glutathione S-Transferase Gene Family in Gossypium raimondii and G. arboreum: Comparative Genomic Study and their Expression under Salt Stress
Auteurs : Yating Dong ; Cong Li ; Yi Zhang ; Qiuling He ; Muhammad K. Daud ; Jinhong Chen ; Shuijin ZhuSource :
- Frontiers in Plant Science [ 1664-462X ] ; 2016.
Abstract
Glutathione S-transferases (GSTs) play versatile functions in multiple aspects of plant growth and development. A comprehensive genome-wide survey of this gene family in the genomes of
Url:
DOI: 10.3389/fpls.2016.00139
PubMed: 26904090
PubMed Central: 4751282
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Glutathione S-Transferase Gene Family in <italic>Gossypium raimondii</italic> and <italic>G. arboreum</italic>: Comparative Genomic Study and their Expression under Salt Stress</title><author><name sortKey="Dong, Yating" sort="Dong, Yating" uniqKey="Dong Y" first="Yating" last="Dong">Yating Dong</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Li, Cong" sort="Li, Cong" uniqKey="Li C" first="Cong" last="Li">Cong Li</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Zhang, Yi" sort="Zhang, Yi" uniqKey="Zhang Y" first="Yi" last="Zhang">Yi Zhang</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="He, Qiuling" sort="He, Qiuling" uniqKey="He Q" first="Qiuling" last="He">Qiuling He</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Daud, Muhammad K" sort="Daud, Muhammad K" uniqKey="Daud M" first="Muhammad K." last="Daud">Muhammad K. Daud</name><affiliation><nlm:aff id="aff2"><institution>Department of Biotechnology and Genetic Engineering, Kohat University of Science and Technology</institution><country>Kohat, Pakistan</country></nlm:aff></affiliation></author><author><name sortKey="Chen, Jinhong" sort="Chen, Jinhong" uniqKey="Chen J" first="Jinhong" last="Chen">Jinhong Chen</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Zhu, Shuijin" sort="Zhu, Shuijin" uniqKey="Zhu S" first="Shuijin" last="Zhu">Shuijin Zhu</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26904090</idno><idno type="pmc">4751282</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4751282</idno><idno type="RBID">PMC:4751282</idno><idno type="doi">10.3389/fpls.2016.00139</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000302</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Glutathione S-Transferase Gene Family in <italic>Gossypium raimondii</italic> and <italic>G. arboreum</italic>: Comparative Genomic Study and their Expression under Salt Stress</title><author><name sortKey="Dong, Yating" sort="Dong, Yating" uniqKey="Dong Y" first="Yating" last="Dong">Yating Dong</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Li, Cong" sort="Li, Cong" uniqKey="Li C" first="Cong" last="Li">Cong Li</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Zhang, Yi" sort="Zhang, Yi" uniqKey="Zhang Y" first="Yi" last="Zhang">Yi Zhang</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="He, Qiuling" sort="He, Qiuling" uniqKey="He Q" first="Qiuling" last="He">Qiuling He</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Daud, Muhammad K" sort="Daud, Muhammad K" uniqKey="Daud M" first="Muhammad K." last="Daud">Muhammad K. Daud</name><affiliation><nlm:aff id="aff2"><institution>Department of Biotechnology and Genetic Engineering, Kohat University of Science and Technology</institution><country>Kohat, Pakistan</country></nlm:aff></affiliation></author><author><name sortKey="Chen, Jinhong" sort="Chen, Jinhong" uniqKey="Chen J" first="Jinhong" last="Chen">Jinhong Chen</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author><author><name sortKey="Zhu, Shuijin" sort="Zhu, Shuijin" uniqKey="Zhu S" first="Shuijin" last="Zhu">Shuijin Zhu</name><affiliation><nlm:aff id="aff1"><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Plant Science</title><idno type="eISSN">1664-462X</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Glutathione S-transferases (GSTs) play versatile functions in multiple aspects of plant growth and development. A comprehensive genome-wide survey of this gene family in the genomes of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> was carried out in this study. Based on phylogenetic analyses, the <italic>GST</italic> gene family of both two diploid cotton species could be divided into eight classes, and approximately all the <italic>GST</italic> genes within the same subfamily shared similar gene structure. Additionally, the gene structures between the orthologs were highly conserved. The chromosomal localization analyses revealed that <italic>GST</italic> genes were unevenly distributed across the genome in both <italic>G. raimondii</italic> and <italic>G. arboreum</italic>. Tandem duplication could be the major driver for the expansion of <italic>GST</italic> gene families. Meanwhile, the expression analysis for the selected 40 <italic>GST</italic> genes showed that they exhibited tissue-specific expression patterns and their expression were induced or repressed by salt stress. Those findings shed lights on the function and evolution of the <italic>GST</italic> gene family in <italic>Gossypium</italic> species.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Armstrong, R N" uniqKey="Armstrong R">R. N. Armstrong</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bjellqvist, B" uniqKey="Bjellqvist B">B. Bjellqvist</name></author><author><name sortKey="Basse, B" uniqKey="Basse B">B. Basse</name></author><author><name sortKey="Olsen, E" uniqKey="Olsen E">E. Olsen</name></author><author><name sortKey="Celis, J E" uniqKey="Celis J">J. E. Celis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Blanc, G" uniqKey="Blanc G">G. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id><journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id><journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id><journal-title-group><journal-title>Frontiers in Plant Science</journal-title></journal-title-group><issn pub-type="epub">1664-462X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26904090</article-id><article-id pub-id-type="pmc">4751282</article-id><article-id pub-id-type="doi">10.3389/fpls.2016.00139</article-id><article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject><subj-group><subject>Original Research</subject></subj-group></subj-group></article-categories><title-group><article-title>Glutathione S-Transferase Gene Family in <italic>Gossypium raimondii</italic> and <italic>G. arboreum</italic>: Comparative Genomic Study and their Expression under Salt Stress</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Dong</surname><given-names>Yating</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/297857/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Cong</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/317700/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Yi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/308033/overview"></uri></contrib><contrib contrib-type="author"><name><surname>He</surname><given-names>Qiuling</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Daud</surname><given-names>Muhammad K.</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/119280/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Jinhong</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/317681/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Zhu</surname><given-names>Shuijin</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn002"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/300347/overview"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Department of Agronomy, Zhejiang University</institution><country>Hangzhou, China</country></aff><aff id="aff2"><sup>2</sup><institution>Department of Biotechnology and Genetic Engineering, Kohat University of Science and Technology</institution><country>Kohat, Pakistan</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Paula Casati, Centro de Estudios Fotosintéticos y Bioquímicos-CONICET, Argentina</p></fn><fn fn-type="edited-by"><p>Reviewed by: Sebastian Pablo Rius, Centro de Estudios Fotosintéticos y Bioquímicos-CONICET, Argentina; Caiguo Zhang, University of Colorado, Denver, USA</p></fn><corresp id="fn001">*Correspondence: Jinhong Chen <email xlink:type="simple">jinhongchen@zju.edu.cn</email>;</corresp><corresp id="fn002">Shuijin Zhu <email xlink:type="simple">shjzhu@zju.edu.cn</email></corresp><fn fn-type="other" id="fn003"><p>This article was submitted to Plant Genetics and Genomics, a section of the journal Frontiers in Plant Science</p></fn></author-notes><pub-date pub-type="epub"><day>12</day><month>2</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>7</volume><elocation-id>139</elocation-id><history><date date-type="received"><day>11</day><month>12</month><year>2015</year></date><date date-type="accepted"><day>27</day><month>1</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016 Dong, Li, Zhang, He, Daud, Chen and Zhu.</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Dong, Li, Zhang, He, Daud, Chen and Zhu</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Glutathione S-transferases (GSTs) play versatile functions in multiple aspects of plant growth and development. A comprehensive genome-wide survey of this gene family in the genomes of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> was carried out in this study. Based on phylogenetic analyses, the <italic>GST</italic> gene family of both two diploid cotton species could be divided into eight classes, and approximately all the <italic>GST</italic> genes within the same subfamily shared similar gene structure. Additionally, the gene structures between the orthologs were highly conserved. The chromosomal localization analyses revealed that <italic>GST</italic> genes were unevenly distributed across the genome in both <italic>G. raimondii</italic> and <italic>G. arboreum</italic>. Tandem duplication could be the major driver for the expansion of <italic>GST</italic> gene families. Meanwhile, the expression analysis for the selected 40 <italic>GST</italic> genes showed that they exhibited tissue-specific expression patterns and their expression were induced or repressed by salt stress. Those findings shed lights on the function and evolution of the <italic>GST</italic> gene family in <italic>Gossypium</italic> species.</p></abstract><kwd-group><kwd>salt stress</kwd><kwd>cotton</kwd><kwd>phylogenetic analysis</kwd><kwd>gene family</kwd><kwd>GST</kwd></kwd-group><counts><fig-count count="7"></fig-count><table-count count="3"></table-count><equation-count count="0"></equation-count><ref-count count="72"></ref-count><page-count count="16"></page-count><word-count count="9865"></word-count></counts></article-meta></front><body><sec sec-type="intro" id="s1"><title>Introduction</title><p>Glutathione S-transferases (GSTs; EC 2.5.1.18) are ancient and ubiquitous proteins encoded by a large gene family that function versatilely in organism. As a kind of detoxification enzymes, GSTs catalyze the conjugation of the tripeptide glutathione (GSH) to a variety of hydrophobic, electrophilic, and usually cytotoxic exogenous compounds (Marrs, <xref rid="B42" ref-type="bibr">1996</xref>). There are cytosolic, mitochondrial and microsomal GSTs derived from a gene superfamily that are involved in the metabolism of xenobiotics (Armstrong, <xref rid="B1" ref-type="bibr">1997</xref>). In general, microsomal and mitochondrial GSTs show great differences in biosynthesis and sequence identity with cytosolic GSTs (Mohsenzadeh et al., <xref rid="B43" ref-type="bibr">2011</xref>). In plants, most cytosolic GSTs typically function as either heterodimer or homodimer of subunits ranging from 23 to 29 kDa in molecular weight (Frova, <xref rid="B20" ref-type="bibr">2006</xref>). Each subunit contains a conserved GSH-binding site (G-site) in the N-terminal domain and an electrophilic substrate binding site (H-site) located in the C-terminal domain (Edwards et al., <xref rid="B15" ref-type="bibr">2000</xref>). GSTs can also be monomeric, like DHAR and Lambda GST in <italic>Arabidopsis</italic> (Dixon et al., <xref rid="B11" ref-type="bibr">2002</xref>). GSTs comprise ~2% of soluble proteins in plants (Rezaei et al., <xref rid="B51" ref-type="bibr">2013</xref>). Based on gene organization and amino acid sequence similarity, the soluble GSTs can be divided into eight classes, including Phi (F), Tau (U), Lambda (L), dehydroascorbate reductase (DHAR), Theta (T), Zeta (Z), γ-subunit of translation elongation factor 1B (EF1Bγ), and tetrachlorohydroquinone dehalogenase (TCHQD; Sheehan et al., <xref rid="B57" ref-type="bibr">2001</xref>; Dixon et al., <xref rid="B11" ref-type="bibr">2002</xref>; Liu et al., <xref rid="B37" ref-type="bibr">2013</xref>). Among these, the first four classes are specific to plant. Genome-wide analyses have indicated that there were 55 <italic>GST</italic> genes in <italic>Arabidopsis</italic> (Sappl et al., <xref rid="B53" ref-type="bibr">2009</xref>), 79 in rice (Soranzo et al., <xref rid="B59" ref-type="bibr">2004</xref>; Jain et al., <xref rid="B27" ref-type="bibr">2010</xref>), 84 in barley (Rezaei et al., <xref rid="B51" ref-type="bibr">2013</xref>), 23 in sweet orange (Licciardello et al., <xref rid="B35" ref-type="bibr">2014</xref>), and 27 in Japanese larch (Yang et al., <xref rid="B67" ref-type="bibr">2014</xref>).</p><p>Since the function for plant GSTs in herbicides detoxification was firstly detected, many researches have focused on their functions under various stimulations. It has been confirmed that GSTs can be induced by plant hormones such as auxins, ABA, and ethylene, as well as biotic and abiotic stresses (Dixon et al., <xref rid="B9" ref-type="bibr">1998</xref>). To date, abundant <italic>GST</italic> genes have been characterized from numerous plant species. Among these <italic>GST</italic> genes, Tau and Phi classes are most investigated probably because of their abundant presence in plant kingdom. <italic>AtGSTU26</italic> in <italic>Arabidopsis</italic> was induced by the chloroacetanilide herbicides, alachlor and metolachlor, the safener benoxacor, and low temperatures (Nutricati et al., <xref rid="B44" ref-type="bibr">2006</xref>). The <italic>OsGSTU5</italic> in rice shown high activity toward chloro-s-triazine and acetanilide herbicides (Cho et al., <xref rid="B7" ref-type="bibr">2006</xref>), and overexpression of <italic>OsGSTU4</italic> in <italic>Arabidopsis</italic> improved the tolerance to salinity and oxidative stresses (Sharma et al., <xref rid="B56" ref-type="bibr">2014</xref>). The expression levels of <italic>TaGSTU1B</italic> and <italic>TaGSTF6</italic> were increased under drought stress in wheat (Galle et al., <xref rid="B21" ref-type="bibr">2009</xref>). Meanwhile, 35 of 56 <italic>SbGSTUs</italic> in Sorghum shown significant response to abiotic stresses including cold, PEG and high salinity (Chi et al., <xref rid="B6" ref-type="bibr">2011</xref>). The expression of <italic>GmGSTL1</italic> from soybean in transgenic <italic>Arabidopsis</italic> could also alleviate the symptoms under salt stress (Chan and Lam, <xref rid="B5" ref-type="bibr">2014</xref>). Many other similar researches on GST family and their functions were reported recently (Urano et al., <xref rid="B63" ref-type="bibr">2000</xref>; Thom et al., <xref rid="B62" ref-type="bibr">2001</xref>; Ma et al., <xref rid="B39" ref-type="bibr">2009</xref>; Ji et al., <xref rid="B28" ref-type="bibr">2010</xref>). However, little is known about this gene family in cotton, especially their function under salt stress.</p><p>Cotton, which belongs to the genus of <italic>Gossypium</italic>, is considered the main source of natural fiber and cultivated worldwide. There are ~45 diploid (2<italic>n</italic> = 2<italic>x</italic> = 26) and 5 tetraploid (2<italic>n</italic> = 4<italic>x</italic> = 52) species. Cotton is an ideal model system for plant polyploid research (Kadir, <xref rid="B29" ref-type="bibr">1976</xref>; Grover et al., <xref rid="B22" ref-type="bibr">2007</xref>). With completion of the genome sequencing of the two diploid cotton species, <italic>G. raimondii</italic> (Paterson et al., <xref rid="B47" ref-type="bibr">2012</xref>; Wang et al., <xref rid="B65" ref-type="bibr">2012</xref>) and <italic>G. arboreum</italic> (Li et al., <xref rid="B33" ref-type="bibr">2014</xref>), genome-wide analyses of all related genes have been realized. <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were the putative donor species for the D and A chromosome groups of tetraploid cotton species, respectively (Kadir, <xref rid="B29" ref-type="bibr">1976</xref>; Grover et al., <xref rid="B22" ref-type="bibr">2007</xref>). Here, we conducted a systematic study of <italic>GST</italic> gene family in <italic>G. raimondii</italic> and <italic>G. arboreum</italic> to identify the characterization and phylogenetic relationships between the two species. Functional diversification and expression profiles of <italic>GST</italic> genes in response to salt stress were also investigated. It may elucidate the evolution mechanism of <italic>GST</italic> gene family in cotton, which will also promote us to perform a further investigation on the stress responsive genes that will provide valuable information for breeding stress-resistant cotton.</p></sec><sec sec-type="materials and methods" id="s2"><title>Materials and methods</title><sec><title>Sequence retrial and annotation of <italic>GST</italic> genes</title><p>The <italic>G. raimondii</italic> genome database (release version 2.1; Paterson et al., <xref rid="B47" ref-type="bibr">2012</xref>) was obtained from Phytozome (<ext-link ext-link-type="uri" xlink:href="http://phytozome.jgi.doe.gov/pz/portal.html#!info?alias=Org_Graimondii">http://phytozome.jgi.doe.gov/pz/portal.html#!info?alias=Org_Graimondii</ext-link>). The published GST proteins of <italic>Arabidopsis</italic> (Sappl et al., <xref rid="B53" ref-type="bibr">2009</xref>) and rice (Soranzo et al., <xref rid="B59" ref-type="bibr">2004</xref>; Jain et al., <xref rid="B27" ref-type="bibr">2010</xref>) were downloaded from the Arabidopsis Information Resource (TAIR release 10, <ext-link ext-link-type="uri" xlink:href="http://www.arabidopsis.org">http://www.arabidopsis.org</ext-link>) and the Rice Genome Annotation Project Database (RGAP release 7, <ext-link ext-link-type="uri" xlink:href="http://rice.plantbiology.msu.edu/index.shtml">http://rice.plantbiology.msu.edu/index.shtml</ext-link>), respectively. Afterwards, they were used as queries in BlastP and tBlastN searches with a stringent <italic>E</italic>-value cut-off (≤ e−20) against the <italic>G. raimondii</italic> genome database. Then, all significant hits were subjected to the InterProScan program (<ext-link ext-link-type="uri" xlink:href="http://www.ebi.ac.uk/Tools/pfa/iprscan/">http://www.ebi.ac.uk/Tools/pfa/iprscan/</ext-link>; Quevillon et al., <xref rid="B50" ref-type="bibr">2005</xref>) to confirm the presence of the conserved domains. Pfam (<ext-link ext-link-type="uri" xlink:href="http://pfam.sanger.ac.uk/">http://pfam.sanger.ac.uk/</ext-link>; Finn et al., <xref rid="B17" ref-type="bibr">2008</xref>, <xref rid="B16" ref-type="bibr">2014</xref>) and SMART (<ext-link ext-link-type="uri" xlink:href="http://smart.embl-heidelberg.de/">http://smart.embl-heidelberg.de/</ext-link>; Letunic et al., <xref rid="B32" ref-type="bibr">2015</xref>) database were applied to further determine each candidate member of the GST family. The same approaches were executed to search against the <italic>G. arboreum</italic> genome database (release version2; Li et al., <xref rid="B33" ref-type="bibr">2014</xref>) which was downloaded from CGP (<ext-link ext-link-type="uri" xlink:href="http://cgp.genomics.org.cn/">http://cgp.genomics.org.cn/</ext-link>) to get the putative homologous <italic>GST</italic> genes. Finally, the physicochemical parameters of the full-length proteins were calculated by Compute pI/Mw tool (<ext-link ext-link-type="uri" xlink:href="http://web.expasy.org/compute_pi/pi_tool">http://web.expasy.org/compute_pi/pi_tool</ext-link>; Bjellqvist et al., <xref rid="B2" ref-type="bibr">1994</xref>), and the subcellular localization prediction was predicted by the CELLO v2.5 server (<ext-link ext-link-type="uri" xlink:href="http://cello.life.nctu.edu.tw/">http://cello.life.nctu.edu.tw/</ext-link>; Yu et al., <xref rid="B68" ref-type="bibr">2004</xref>).</p></sec><sec><title>Phylogenetic analysis and genomic organizations prediction</title><p>Multiple sequence alignments of all full-length GST proteins were performed using MUSCLE 3.52 program (Edgar, <xref rid="B14" ref-type="bibr">2004</xref>) with default parameters, followed by manual comparisons and refinements. Phylogenetic trees were constructed by Neighbor Joining method in MEGA 5.2 (Tamura et al., <xref rid="B60" ref-type="bibr">2011</xref>). Neighbor Joining analyses were carried out using pairwise deletion option and poisson correction model. To assess statistical reliability for each node, bootstrap tests were conducted with 1000 replicates. Furthermore, Minimum Evolution method of MEGA was also applied in the tree construction to validate the results from the NJ method.</p><p>The exon-intron structures were deduced using GSDS (<ext-link ext-link-type="uri" xlink:href="http://gsds.cbi.pku.edu.cn/">http://gsds.cbi.pku.edu.cn/</ext-link>; Hu et al., <xref rid="B26" ref-type="bibr">2015</xref>), through comparing the predicted coding sequences and their corresponding genomic DNA sequences.</p></sec><sec><title>Chromosomal localization and detection of gene duplication</title><p>All the cotton <italic>GST</italic> genes were mapped on the chromosomes according to their starting positions given in the genome annotation document. The chromosome location images were portrayed graphically by MapInspect software.</p><p><italic>GST</italic> gene duplication events were defined according to the length coverage of the longer one between aligned gene sequences and the identity of the aligned regions, and only one duplication event was counted for tightly-linked genes (Maher et al., <xref rid="B40" ref-type="bibr">2006</xref>; Ouyang et al., <xref rid="B46" ref-type="bibr">2009</xref>; Liu et al., <xref rid="B36" ref-type="bibr">2014</xref>). Referring to the different chromosomal location, these <italic>GST</italic> genes were designated as either tandem duplication or segmental duplication.</p></sec><sec><title>Estimating Ka/Ks ratios for duplicated gene pairs</title><p>Firstly, all the full-length gene sequences of the duplicated <italic>GST</italic> gene pairs of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were aligned by Clustal X 2.0 program (Larkin et al., <xref rid="B31" ref-type="bibr">2007</xref>). Subsequently, the nonsynonymous substitutions rate (Ka) and synonymous substitution rate (Ks) were calculated using the software DnaSp V5.0 (Librado and Rozas, <xref rid="B34" ref-type="bibr">2009</xref>). Eventually, the selection pressure of each gene pair was assessed based on the Ka/Ks ratio.</p></sec><sec><title>Promoter regions analysis</title><p>In order to analyze promoter, the 2500 bp genomic DNA sequences upstream of the initiation codon (ATG) were extracted from the genome database. Then, these sequences were subjected to the PLACE database (<ext-link ext-link-type="uri" xlink:href="http://www.dna.affrc.go.jp/PLACE/signalscan.html">http://www.dna.affrc.go.jp/PLACE/signalscan.html</ext-link>; Higo et al., <xref rid="B25" ref-type="bibr">1999</xref>) to search for the putative <italic>cis</italic>-elements in promoter regions.</p></sec><sec><title>Plant materials and salt treatments</title><p>One-week-old cotton seedlings of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were transplanted into polypots (10 cm in diameter) with MS medium and put in a temperature-controlled chamber with temperature of 28°C, relative humidity of 60%, and photoperiod of 16 h light and 8 h dark. After acclimatization for 7 days, they were subjected to salt treatment. For <italic>G. raimondii</italic>, the MS solution were adjusted to desired salt concentrations, i.e., 0, 50, 100, and 200 mM, which represented the control condition, slight stress, moderate stress, and severe stress, respectively. Identically, final salt concentrations for <italic>G. arboreum</italic> were 0, 100, 200, and 300 mM. Three biological replicates were conducted for each sample. After treatments for 2 weeks, the root, stem, cotyledon and leaf were harvested from each individual for expression analysis. All collected samples were immediately frozen in liquid nitrogen and stored at −80°C.</p></sec><sec><title>RNA isolation and real-time quantitative PCR (qRT-PCR) analysis</title><p>Total RNAs of all the collected samples were extracted using EASYspin Plus RNAprep Kit (Aidlab, Beijing, China). The quantity and quality were determined by a NanoDrop 2000 Spectrophotometer (NanoDrop Technologies, Wilmington, DE, USA). First-strand cDNA was synthesized with PrimerScript 1st Strand cDNA synthesis kit (TaKaRa, Dalian, China). All the protocols followed to the manufacturer's instructions. qRT-PCR was performed with Lightcycler 96 system (Roche, Mannheim, Germany) using SYBR the premix Ex taq (TakaRa, Dalian, China) in 20 μL volume according to the supplier's protocols. The specific primers used were listed in Supplementary Table <xref ref-type="supplementary-material" rid="SM4">1</xref>, and cotton <italic>UBQ7</italic> was used as an internal control. Three biological replicates were performed for each sample. The relative expression levels were calculated according to the 2<sup>−ΔΔCt</sup> method (Livak and Schmittgen, <xref rid="B38" ref-type="bibr">2001</xref>). The heatmap for expression profiles were generated with the Mev 4.0 software (Saeed et al., <xref rid="B52" ref-type="bibr">2003</xref>).</p></sec></sec><sec sec-type="results" id="s3"><title>Results</title><sec><title>Characterization of <italic>GST</italic> gene family in <italic>G. raimondii</italic> and <italic>G. arboreum</italic></title><p>The genome-wide analyses of <italic>GST</italic> gene family have been performed on the basis of recently completed two diploid cotton genome sequences, <italic>G. raimondii</italic> (Paterson et al., <xref rid="B47" ref-type="bibr">2012</xref>) and <italic>G. arboreum</italic> (Li et al., <xref rid="B33" ref-type="bibr">2014</xref>). Through a systematic BLAST search against the <italic>G. raimondii</italic> and <italic>G. arboreum</italic> genome databases with the query sequences of <italic>Arabidopsis</italic> (55) and rice (77) GST proteins, the candidate <italic>GST</italic> genes were identified. Among the 79 <italic>GST</italic> genes in rice (Soranzo et al., <xref rid="B59" ref-type="bibr">2004</xref>; Jain et al., <xref rid="B27" ref-type="bibr">2010</xref>), the sequences for two genes (LOC_Os10g38501, <italic>OsGSTU3</italic>; LOC_Os10g38495, <italic>OsGSTU4</italic>) could not be retrieved as they have become obsolete entries in TIGR database. Therefore, the number of rice <italic>GST</italic> genes used as queries was 77. Then, all these retrieved sequences were verified by the Pfam and SMART analyses, and a total of 59 and 49 non-redundant genes containing both typical GST N- and C-terminal domains were confirmed in the <italic>G. raimondii</italic> and <italic>G. arboreum</italic> genome, respectively (Tables <xref ref-type="table" rid="T1">1</xref>, <xref ref-type="table" rid="T2">2</xref>).</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>The information of 59 <italic>GST</italic> genes from <italic>G. raimondii</italic></bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene Name</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene identifier</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Genomics position</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>CDS</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Size (AA)</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold><italic>Mw(kDa)</italic></bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold><italic>pI</italic></bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Predicted Subcellular localization</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Strand</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.001G204000.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 39690577-39691331</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">25.12</td><td valign="top" align="center" rowspan="1" colspan="1">5.66</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.002G166900.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr02: 41370934-41371707</td><td valign="top" align="center" rowspan="1" colspan="1">684</td><td valign="top" align="center" rowspan="1" colspan="1">227</td><td valign="top" align="center" rowspan="1" colspan="1">26.02</td><td valign="top" align="center" rowspan="1" colspan="1">6.4</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.003G127500.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr03: 37860854-37862140</td><td valign="top" align="center" rowspan="1" colspan="1">666</td><td valign="top" align="center" rowspan="1" colspan="1">221</td><td valign="top" align="center" rowspan="1" colspan="1">25.71</td><td valign="top" align="center" rowspan="1" colspan="1">6.03</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU4</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.003G127600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr03: 37865020-37866250</td><td valign="top" align="center" rowspan="1" colspan="1">711</td><td valign="top" align="center" rowspan="1" colspan="1">236</td><td valign="top" align="center" rowspan="1" colspan="1">27.40</td><td valign="top" align="center" rowspan="1" colspan="1">6.61</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU5</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.004G031900.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 2613632-2615489</td><td valign="top" align="center" rowspan="1" colspan="1">723</td><td valign="top" align="center" rowspan="1" colspan="1">240</td><td valign="top" align="center" rowspan="1" colspan="1">26.84</td><td valign="top" align="center" rowspan="1" colspan="1">6.23</td><td valign="top" align="left" rowspan="1" colspan="1">Plasma Membrane</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU6</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.004G032100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 2626962-2628597</td><td valign="top" align="center" rowspan="1" colspan="1">723</td><td valign="top" align="center" rowspan="1" colspan="1">240</td><td valign="top" align="center" rowspan="1" colspan="1">26.76</td><td valign="top" align="center" rowspan="1" colspan="1">6.98</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU7</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G036300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3450978-3452932</td><td valign="top" align="center" rowspan="1" colspan="1">744</td><td valign="top" align="center" rowspan="1" colspan="1">247</td><td valign="top" align="center" rowspan="1" colspan="1">29.10</td><td valign="top" align="center" rowspan="1" colspan="1">8.49</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU8</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G037700.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3540959-3542789</td><td valign="top" align="center" rowspan="1" colspan="1">675</td><td valign="top" align="center" rowspan="1" colspan="1">224</td><td valign="top" align="center" rowspan="1" colspan="1">26.47</td><td valign="top" align="center" rowspan="1" colspan="1">6.09</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU9</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G037800.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3544165-3545392</td><td valign="top" align="center" rowspan="1" colspan="1">675</td><td valign="top" align="center" rowspan="1" colspan="1">224</td><td valign="top" align="center" rowspan="1" colspan="1">26.38</td><td valign="top" align="center" rowspan="1" colspan="1">6.09</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU10</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G037900.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3566839-3573242</td><td valign="top" align="center" rowspan="1" colspan="1">672</td><td valign="top" align="center" rowspan="1" colspan="1">223</td><td valign="top" align="center" rowspan="1" colspan="1">25.73</td><td valign="top" align="center" rowspan="1" colspan="1">5.77</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU11</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G038200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3598187-3600069</td><td valign="top" align="center" rowspan="1" colspan="1">678</td><td valign="top" align="center" rowspan="1" colspan="1">225</td><td valign="top" align="center" rowspan="1" colspan="1">26.53</td><td valign="top" align="center" rowspan="1" colspan="1">6.13</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU12</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G038500.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3628470-3631039</td><td valign="top" align="center" rowspan="1" colspan="1">672</td><td valign="top" align="center" rowspan="1" colspan="1">223</td><td valign="top" align="center" rowspan="1" colspan="1">25.78</td><td valign="top" align="center" rowspan="1" colspan="1">5.42</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU13</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G038700.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3671704-3675708</td><td valign="top" align="center" rowspan="1" colspan="1">669</td><td valign="top" align="center" rowspan="1" colspan="1">222</td><td valign="top" align="center" rowspan="1" colspan="1">25.84</td><td valign="top" align="center" rowspan="1" colspan="1">6.18</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU14</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.005G038800.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 3683779-3685218</td><td valign="top" align="center" rowspan="1" colspan="1">630</td><td valign="top" align="center" rowspan="1" colspan="1">209</td><td valign="top" align="center" rowspan="1" colspan="1">24.31</td><td valign="top" align="center" rowspan="1" colspan="1">7.13</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU15</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.006G178400.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr06: 43579129-43580293</td><td valign="top" align="center" rowspan="1" colspan="1">654</td><td valign="top" align="center" rowspan="1" colspan="1">217</td><td valign="top" align="center" rowspan="1" colspan="1">24.79</td><td valign="top" align="center" rowspan="1" colspan="1">5.26</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU16</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.006G178600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr06: 43599284-43600758</td><td valign="top" align="center" rowspan="1" colspan="1">678</td><td valign="top" align="center" rowspan="1" colspan="1">225</td><td valign="top" align="center" rowspan="1" colspan="1">25.85</td><td valign="top" align="center" rowspan="1" colspan="1">5.75</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU17</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.006G178700.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr06: 43603138-43603967</td><td valign="top" align="center" rowspan="1" colspan="1">594</td><td valign="top" align="center" rowspan="1" colspan="1">197</td><td valign="top" align="center" rowspan="1" colspan="1">22.25</td><td valign="top" align="center" rowspan="1" colspan="1">5.53</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU18</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G072000.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 5072423-5074861</td><td valign="top" align="center" rowspan="1" colspan="1">702</td><td valign="top" align="center" rowspan="1" colspan="1">233</td><td valign="top" align="center" rowspan="1" colspan="1">26.13</td><td valign="top" align="center" rowspan="1" colspan="1">8.67</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU19</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G151400.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 12969311-12970236</td><td valign="top" align="center" rowspan="1" colspan="1">672</td><td valign="top" align="center" rowspan="1" colspan="1">223</td><td valign="top" align="center" rowspan="1" colspan="1">25.82</td><td valign="top" align="center" rowspan="1" colspan="1">5.61</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU20</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G245500.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 36874442-36875934</td><td valign="top" align="center" rowspan="1" colspan="1">699</td><td valign="top" align="center" rowspan="1" colspan="1">232</td><td valign="top" align="center" rowspan="1" colspan="1">26.06</td><td valign="top" align="center" rowspan="1" colspan="1">6.01</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU21</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G249200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 39160450-39161476</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">25.32</td><td valign="top" align="center" rowspan="1" colspan="1">5.52</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU22</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G348100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 57798231-57800653</td><td valign="top" align="center" rowspan="1" colspan="1">627</td><td valign="top" align="center" rowspan="1" colspan="1">208</td><td valign="top" align="center" rowspan="1" colspan="1">24.65</td><td valign="top" align="center" rowspan="1" colspan="1">9.35</td><td valign="top" align="left" rowspan="1" colspan="1">Mitochondrial</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU23</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.009G357800.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr09: 46937960-46939545</td><td valign="top" align="center" rowspan="1" colspan="1">666</td><td valign="top" align="center" rowspan="1" colspan="1">221</td><td valign="top" align="center" rowspan="1" colspan="1">25.79</td><td valign="top" align="center" rowspan="1" colspan="1">5.72</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU24</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.010G115400.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr10: 22318160-22318790</td><td valign="top" align="center" rowspan="1" colspan="1">585</td><td valign="top" align="center" rowspan="1" colspan="1">194</td><td valign="top" align="center" rowspan="1" colspan="1">22.72</td><td valign="top" align="center" rowspan="1" colspan="1">6.12</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU25</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.011G163600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 31290617-31297277</td><td valign="top" align="center" rowspan="1" colspan="1">675</td><td valign="top" align="center" rowspan="1" colspan="1">224</td><td valign="top" align="center" rowspan="1" colspan="1">26.10</td><td valign="top" align="center" rowspan="1" colspan="1">5.92</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU26</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.012G099100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 21014065-21015298</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">25.46</td><td valign="top" align="center" rowspan="1" colspan="1">6.03</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU27</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.012G120900.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 27604435-27605617</td><td valign="top" align="center" rowspan="1" colspan="1">705</td><td valign="top" align="center" rowspan="1" colspan="1">234</td><td valign="top" align="center" rowspan="1" colspan="1">26.09</td><td valign="top" align="center" rowspan="1" colspan="1">6.45</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU28</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.012G121000.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 27610911-27612136</td><td valign="top" align="center" rowspan="1" colspan="1">705</td><td valign="top" align="center" rowspan="1" colspan="1">234</td><td valign="top" align="center" rowspan="1" colspan="1">25.95</td><td valign="top" align="center" rowspan="1" colspan="1">5.36</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU29</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.012G121100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 27617631-27619108</td><td valign="top" align="center" rowspan="1" colspan="1">705</td><td valign="top" align="center" rowspan="1" colspan="1">234</td><td valign="top" align="center" rowspan="1" colspan="1">25.92</td><td valign="top" align="center" rowspan="1" colspan="1">5.25</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU30</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.012G121400.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 27665597-27666786</td><td valign="top" align="center" rowspan="1" colspan="1">711</td><td valign="top" align="center" rowspan="1" colspan="1">236</td><td valign="top" align="center" rowspan="1" colspan="1">26.16</td><td valign="top" align="center" rowspan="1" colspan="1">5.76</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU31</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G014600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 997489-999065</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">24.48</td><td valign="top" align="center" rowspan="1" colspan="1">5.26</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU32</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G112700.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 26930123-26930852</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.63</td><td valign="top" align="center" rowspan="1" colspan="1">7.17</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU33</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G113600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 27659031-27660061</td><td valign="top" align="center" rowspan="1" colspan="1">681</td><td valign="top" align="center" rowspan="1" colspan="1">226</td><td valign="top" align="center" rowspan="1" colspan="1">25.74</td><td valign="top" align="center" rowspan="1" colspan="1">5.29</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU34</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G177200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 46961394-46962365</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.17</td><td valign="top" align="center" rowspan="1" colspan="1">6.53</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU35</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G177300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 47002219-47003549</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.46</td><td valign="top" align="center" rowspan="1" colspan="1">6.84</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU36</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G177400.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 47013066-47013998</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.89</td><td valign="top" align="center" rowspan="1" colspan="1">6.25</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU37</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G177600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 47037500-47039519</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.43</td><td valign="top" align="center" rowspan="1" colspan="1">5.58</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU38</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G179300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 47275362-47277951</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.44</td><td valign="top" align="center" rowspan="1" colspan="1">6.9</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.001G083600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 8834222-8836505</td><td valign="top" align="center" rowspan="1" colspan="1">645</td><td valign="top" align="center" rowspan="1" colspan="1">214</td><td valign="top" align="center" rowspan="1" colspan="1">24.58</td><td valign="top" align="center" rowspan="1" colspan="1">5.76</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.004G141900.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 40004892-40006445</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.33</td><td valign="top" align="center" rowspan="1" colspan="1">6.19</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G129400.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 10398983-10400208</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">24.79</td><td valign="top" align="center" rowspan="1" colspan="1">5.42</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF4</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G175100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 16220916-16222730</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.79</td><td valign="top" align="center" rowspan="1" colspan="1">5.34</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF5</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G240200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 33067227-33069528</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">24.68</td><td valign="top" align="center" rowspan="1" colspan="1">8.35</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF6</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.008G010200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 1197081-1198882</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.07</td><td valign="top" align="center" rowspan="1" colspan="1">6.13</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTF7</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.011G211600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 51061907-51062856</td><td valign="top" align="center" rowspan="1" colspan="1">697</td><td valign="top" align="center" rowspan="1" colspan="1">198</td><td valign="top" align="center" rowspan="1" colspan="1">22.30</td><td valign="top" align="center" rowspan="1" colspan="1">5.82</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTT1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.004G211100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 54407517-54410688</td><td valign="top" align="center" rowspan="1" colspan="1">837</td><td valign="top" align="center" rowspan="1" colspan="1">278</td><td valign="top" align="center" rowspan="1" colspan="1">31.95</td><td valign="top" align="center" rowspan="1" colspan="1">9.52</td><td valign="top" align="left" rowspan="1" colspan="1">Mitochondrial</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTT2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.007G023300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 1661709-1664000</td><td valign="top" align="center" rowspan="1" colspan="1">756</td><td valign="top" align="center" rowspan="1" colspan="1">251</td><td valign="top" align="center" rowspan="1" colspan="1">28.50</td><td valign="top" align="center" rowspan="1" colspan="1">9.37</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTT3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.008G246300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 53071831-53074716</td><td valign="top" align="center" rowspan="1" colspan="1">753</td><td valign="top" align="center" rowspan="1" colspan="1">250</td><td valign="top" align="center" rowspan="1" colspan="1">28.31</td><td valign="top" align="center" rowspan="1" colspan="1">9.49</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTZ1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.008G114200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 34672415-34675860</td><td valign="top" align="center" rowspan="1" colspan="1">774</td><td valign="top" align="center" rowspan="1" colspan="1">257</td><td valign="top" align="center" rowspan="1" colspan="1">28.90</td><td valign="top" align="center" rowspan="1" colspan="1">5.72</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTZ2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.011G090100.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 9558249-9561007</td><td valign="top" align="center" rowspan="1" colspan="1">657</td><td valign="top" align="center" rowspan="1" colspan="1">218</td><td valign="top" align="center" rowspan="1" colspan="1">24.73</td><td valign="top" align="center" rowspan="1" colspan="1">5.21</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTL1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.002G252300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr02: 61557665-61560819</td><td valign="top" align="center" rowspan="1" colspan="1">738</td><td valign="top" align="center" rowspan="1" colspan="1">245</td><td valign="top" align="center" rowspan="1" colspan="1">28.26</td><td valign="top" align="center" rowspan="1" colspan="1">5.32</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTL2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.006G177600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr06: 43499453-43502034</td><td valign="top" align="center" rowspan="1" colspan="1">714</td><td valign="top" align="center" rowspan="1" colspan="1">237</td><td valign="top" align="center" rowspan="1" colspan="1">26.93</td><td valign="top" align="center" rowspan="1" colspan="1">5.12</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTL3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G024200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 1770849 1774598</td><td valign="top" align="center" rowspan="1" colspan="1">969</td><td valign="top" align="center" rowspan="1" colspan="1">322</td><td valign="top" align="center" rowspan="1" colspan="1">36.58</td><td valign="top" align="center" rowspan="1" colspan="1">7.6</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrEF1Bγ1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.008G046200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 6226741-6230087</td><td valign="top" align="center" rowspan="1" colspan="1">1266</td><td valign="top" align="center" rowspan="1" colspan="1">421</td><td valign="top" align="center" rowspan="1" colspan="1">47.69</td><td valign="top" align="center" rowspan="1" colspan="1">7.53</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrEF1Bγ2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.008G046300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 6259415 6262692</td><td valign="top" align="center" rowspan="1" colspan="1">1266</td><td valign="top" align="center" rowspan="1" colspan="1">421</td><td valign="top" align="center" rowspan="1" colspan="1">47.69</td><td valign="top" align="center" rowspan="1" colspan="1">7.53</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrDHAR1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.001G089300.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 9656330-9658909</td><td valign="top" align="center" rowspan="1" colspan="1">789</td><td valign="top" align="center" rowspan="1" colspan="1">262</td><td valign="top" align="center" rowspan="1" colspan="1">29.24</td><td valign="top" align="center" rowspan="1" colspan="1">8.79</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrDHAR2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.011G246200.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 57230753-57234321</td><td valign="top" align="center" rowspan="1" colspan="1">639</td><td valign="top" align="center" rowspan="1" colspan="1">212</td><td valign="top" align="center" rowspan="1" colspan="1">23.54</td><td valign="top" align="center" rowspan="1" colspan="1">6.17</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrDHAR3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.012G068600.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 10022598-10024825</td><td valign="top" align="center" rowspan="1" colspan="1">639</td><td valign="top" align="center" rowspan="1" colspan="1">212</td><td valign="top" align="center" rowspan="1" colspan="1">23.47</td><td valign="top" align="center" rowspan="1" colspan="1">6.96</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrTCHQD1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Gorai.013G108000.1</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 23436664 23439362</td><td valign="top" align="center" rowspan="1" colspan="1">798</td><td valign="top" align="center" rowspan="1" colspan="1">265</td><td valign="top" align="center" rowspan="1" colspan="1">30.94</td><td valign="top" align="center" rowspan="1" colspan="1">9.27</td><td valign="top" align="left" rowspan="1" colspan="1">Nuclear</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr></tbody></table></table-wrap><table-wrap id="T2" position="float"><label>Table 2</label><caption><p><bold>The information of 49 <italic>GST</italic> genes from <italic>G. arboreum</italic></bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene name</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Gene identifier</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Genomics position</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>CDS</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Size(AA)</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold><italic>Mw(kDa)</italic></bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold><italic>pI</italic></bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Preditced subcellular localization</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Strand</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_37696</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 115962251-115962956</td><td valign="top" align="center" rowspan="1" colspan="1">612</td><td valign="top" align="center" rowspan="1" colspan="1">203</td><td valign="top" align="center" rowspan="1" colspan="1">23.12</td><td valign="top" align="center" rowspan="1" colspan="1">5.42</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_05897</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 141131040-141131830</td><td valign="top" align="center" rowspan="1" colspan="1">687</td><td valign="top" align="center" rowspan="1" colspan="1">228</td><td valign="top" align="center" rowspan="1" colspan="1">26.56</td><td valign="top" align="center" rowspan="1" colspan="1">5.79</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_36350</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 36480986-36481718</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">25.34</td><td valign="top" align="center" rowspan="1" colspan="1">5.69</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU4</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_19149</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 77946780-77947175</td><td valign="top" align="center" rowspan="1" colspan="1">396</td><td valign="top" align="center" rowspan="1" colspan="1">131</td><td valign="top" align="center" rowspan="1" colspan="1">15.40</td><td valign="top" align="center" rowspan="1" colspan="1">9.48</td><td valign="top" align="left" rowspan="1" colspan="1">Mitochondrial</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU5</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_24534</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 56685154-56687068</td><td valign="top" align="center" rowspan="1" colspan="1">675</td><td valign="top" align="center" rowspan="1" colspan="1">224</td><td valign="top" align="center" rowspan="1" colspan="1">26.24</td><td valign="top" align="center" rowspan="1" colspan="1">5.92</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU6</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_24526</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 56775166-56776607</td><td valign="top" align="center" rowspan="1" colspan="1">678</td><td valign="top" align="center" rowspan="1" colspan="1">225</td><td valign="top" align="center" rowspan="1" colspan="1">26.59</td><td valign="top" align="center" rowspan="1" colspan="1">6.56</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU7</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_24525</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 56779832-56780826</td><td valign="top" align="center" rowspan="1" colspan="1">675</td><td valign="top" align="center" rowspan="1" colspan="1">224</td><td valign="top" align="center" rowspan="1" colspan="1">26.33</td><td valign="top" align="center" rowspan="1" colspan="1">6.08</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU8</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_24523</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 56804944-56807155</td><td valign="top" align="center" rowspan="1" colspan="1">672</td><td valign="top" align="center" rowspan="1" colspan="1">223</td><td valign="top" align="center" rowspan="1" colspan="1">25.82</td><td valign="top" align="center" rowspan="1" colspan="1">5.88</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU9</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_24522</td><td valign="top" align="center" rowspan="1" colspan="1">Chr05: 56808079-56810315</td><td valign="top" align="center" rowspan="1" colspan="1">672</td><td valign="top" align="center" rowspan="1" colspan="1">223</td><td valign="top" align="center" rowspan="1" colspan="1">25.77</td><td valign="top" align="center" rowspan="1" colspan="1">5.1</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU10</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_27775</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 34539787-34541185</td><td valign="top" align="center" rowspan="1" colspan="1">639</td><td valign="top" align="center" rowspan="1" colspan="1">212</td><td valign="top" align="center" rowspan="1" colspan="1">24.72</td><td valign="top" align="center" rowspan="1" colspan="1">5.82</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU11</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_27774</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 34545395-34546394</td><td valign="top" align="center" rowspan="1" colspan="1">711</td><td valign="top" align="center" rowspan="1" colspan="1">236</td><td valign="top" align="center" rowspan="1" colspan="1">27.46</td><td valign="top" align="center" rowspan="1" colspan="1">7.84</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU12</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_34756</td><td valign="top" align="center" rowspan="1" colspan="1">Chr09: 44598342-44600496</td><td valign="top" align="center" rowspan="1" colspan="1">798</td><td valign="top" align="center" rowspan="1" colspan="1">265</td><td valign="top" align="center" rowspan="1" colspan="1">30.51</td><td valign="top" align="center" rowspan="1" colspan="1">5.18</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU13</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_29359</td><td valign="top" align="center" rowspan="1" colspan="1">Chr10: 83946177-83947060</td><td valign="top" align="center" rowspan="1" colspan="1">699</td><td valign="top" align="center" rowspan="1" colspan="1">232</td><td valign="top" align="center" rowspan="1" colspan="1">26.86</td><td valign="top" align="center" rowspan="1" colspan="1">8.68</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU14</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_29361</td><td valign="top" align="center" rowspan="1" colspan="1">Chr10: 84019904-84020941</td><td valign="top" align="center" rowspan="1" colspan="1">519</td><td valign="top" align="center" rowspan="1" colspan="1">172</td><td valign="top" align="center" rowspan="1" colspan="1">19.84</td><td valign="top" align="center" rowspan="1" colspan="1">8.56</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU15</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_29364</td><td valign="top" align="center" rowspan="1" colspan="1">Chr10: 84167770-84168839</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">25.70</td><td valign="top" align="center" rowspan="1" colspan="1">5.42</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU16</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_02462</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 21179427-21180580</td><td valign="top" align="center" rowspan="1" colspan="1">651</td><td valign="top" align="center" rowspan="1" colspan="1">216</td><td valign="top" align="center" rowspan="1" colspan="1">24.69</td><td valign="top" align="center" rowspan="1" colspan="1">6.14</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU17</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_02461</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 21188528-21189567</td><td valign="top" align="center" rowspan="1" colspan="1">678</td><td valign="top" align="center" rowspan="1" colspan="1">225</td><td valign="top" align="center" rowspan="1" colspan="1">25.85</td><td valign="top" align="center" rowspan="1" colspan="1">5.75</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU18</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_02460</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 21222441-21223570</td><td valign="top" align="center" rowspan="1" colspan="1">771</td><td valign="top" align="center" rowspan="1" colspan="1">256</td><td valign="top" align="center" rowspan="1" colspan="1">29.17</td><td valign="top" align="center" rowspan="1" colspan="1">7.6</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU19</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_35955</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 46995035-46995773</td><td valign="top" align="center" rowspan="1" colspan="1">663</td><td valign="top" align="center" rowspan="1" colspan="1">220</td><td valign="top" align="center" rowspan="1" colspan="1">25.92</td><td valign="top" align="center" rowspan="1" colspan="1">6.13</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU20</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_03413</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 26107909-26108689</td><td valign="top" align="center" rowspan="1" colspan="1">711</td><td valign="top" align="center" rowspan="1" colspan="1">236</td><td valign="top" align="center" rowspan="1" colspan="1">26.15</td><td valign="top" align="center" rowspan="1" colspan="1">5.77</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU21</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_03415</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 26129084-26129876</td><td valign="top" align="center" rowspan="1" colspan="1">705</td><td valign="top" align="center" rowspan="1" colspan="1">234</td><td valign="top" align="center" rowspan="1" colspan="1">26.11</td><td valign="top" align="center" rowspan="1" colspan="1">5.53</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU22</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_03416</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 26135225-26136027</td><td valign="top" align="center" rowspan="1" colspan="1">705</td><td valign="top" align="center" rowspan="1" colspan="1">234</td><td valign="top" align="center" rowspan="1" colspan="1">25.81</td><td valign="top" align="center" rowspan="1" colspan="1">5.73</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU23</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_21914</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 56682472-56683218</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.09</td><td valign="top" align="center" rowspan="1" colspan="1">6.53</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU24</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_21915</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 56711009-56711617</td><td valign="top" align="center" rowspan="1" colspan="1">522</td><td valign="top" align="center" rowspan="1" colspan="1">173</td><td valign="top" align="center" rowspan="1" colspan="1">20.17</td><td valign="top" align="center" rowspan="1" colspan="1">7.62</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU25</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_21916</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 56723260-56724010</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.57</td><td valign="top" align="center" rowspan="1" colspan="1">6.91</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU26</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_21917</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 56759324-56760726</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">25.41</td><td valign="top" align="center" rowspan="1" colspan="1">5.58</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU27</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_21938</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 57062669-57063763</td><td valign="top" align="center" rowspan="1" colspan="1">612</td><td valign="top" align="center" rowspan="1" colspan="1">203</td><td valign="top" align="center" rowspan="1" colspan="1">23.53</td><td valign="top" align="center" rowspan="1" colspan="1">8.47</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU28</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_01020</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 74881033-74882362</td><td valign="top" align="center" rowspan="1" colspan="1">669</td><td valign="top" align="center" rowspan="1" colspan="1">222</td><td valign="top" align="center" rowspan="1" colspan="1">24.74</td><td valign="top" align="center" rowspan="1" colspan="1">5.27</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU29</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_35457</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 88582069-88582846</td><td valign="top" align="center" rowspan="1" colspan="1">675</td><td valign="top" align="center" rowspan="1" colspan="1">224</td><td valign="top" align="center" rowspan="1" colspan="1">25.49</td><td valign="top" align="center" rowspan="1" colspan="1">5.28</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTF1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_12201</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 84548715-84550731</td><td valign="top" align="center" rowspan="1" colspan="1">645</td><td valign="top" align="center" rowspan="1" colspan="1">214</td><td valign="top" align="center" rowspan="1" colspan="1">24.57</td><td valign="top" align="center" rowspan="1" colspan="1">5.97</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTF2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_22529</td><td valign="top" align="center" rowspan="1" colspan="1">Chr03: 75186297-75187194</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.34</td><td valign="top" align="center" rowspan="1" colspan="1">6.05</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTF3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_12321</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 23049823-23051175</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.77</td><td valign="top" align="center" rowspan="1" colspan="1">5.46</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTF4</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_23310</td><td valign="top" align="center" rowspan="1" colspan="1">Chr04: 26934603-26935467</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">24.83</td><td valign="top" align="center" rowspan="1" colspan="1">5.41</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTF5</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_34119</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 36371353-36372180</td><td valign="top" align="center" rowspan="1" colspan="1">660</td><td valign="top" align="center" rowspan="1" colspan="1">219</td><td valign="top" align="center" rowspan="1" colspan="1">26.64</td><td valign="top" align="center" rowspan="1" colspan="1">8.67</td><td valign="top" align="left" rowspan="1" colspan="1">Nuclear</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTF6</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_34451</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 48647504-48648924</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.09</td><td valign="top" align="center" rowspan="1" colspan="1">6.44</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTT1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_25983</td><td valign="top" align="center" rowspan="1" colspan="1">Chr03: 24938613-24940995</td><td valign="top" align="center" rowspan="1" colspan="1">753</td><td valign="top" align="center" rowspan="1" colspan="1">250</td><td valign="top" align="center" rowspan="1" colspan="1">28.73</td><td valign="top" align="center" rowspan="1" colspan="1">8.99</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTT2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_14469</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 47840336-47842724</td><td valign="top" align="center" rowspan="1" colspan="1">753</td><td valign="top" align="center" rowspan="1" colspan="1">250</td><td valign="top" align="center" rowspan="1" colspan="1">28.39</td><td valign="top" align="center" rowspan="1" colspan="1">9.45</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTT3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_02311</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 22362230-22367274</td><td valign="top" align="center" rowspan="1" colspan="1">753</td><td valign="top" align="center" rowspan="1" colspan="1">251</td><td valign="top" align="center" rowspan="1" colspan="1">28.37</td><td valign="top" align="center" rowspan="1" colspan="1">8.79</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTZ1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_40149</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 87761510-87763550</td><td valign="top" align="center" rowspan="1" colspan="1">648</td><td valign="top" align="center" rowspan="1" colspan="1">215</td><td valign="top" align="center" rowspan="1" colspan="1">24.37</td><td valign="top" align="center" rowspan="1" colspan="1">5.34</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTZ2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_03363</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 24422813-24429189</td><td valign="top" align="center" rowspan="1" colspan="1">1245</td><td valign="top" align="center" rowspan="1" colspan="1">414</td><td valign="top" align="center" rowspan="1" colspan="1">47.39</td><td valign="top" align="center" rowspan="1" colspan="1">5.6</td><td valign="top" align="left" rowspan="1" colspan="1">Plasma Membrane</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTL1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_00425</td><td valign="top" align="center" rowspan="1" colspan="1">Chr02: 69229452-69232705</td><td valign="top" align="center" rowspan="1" colspan="1">717</td><td valign="top" align="center" rowspan="1" colspan="1">238</td><td valign="top" align="center" rowspan="1" colspan="1">27.46</td><td valign="top" align="center" rowspan="1" colspan="1">5.32</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTL2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_02453</td><td valign="top" align="center" rowspan="1" colspan="1">Chr11: 21297228-21299341</td><td valign="top" align="center" rowspan="1" colspan="1">774</td><td valign="top" align="center" rowspan="1" colspan="1">257</td><td valign="top" align="center" rowspan="1" colspan="1">29.24</td><td valign="top" align="center" rowspan="1" colspan="1">4.82</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTL3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_00921</td><td valign="top" align="center" rowspan="1" colspan="1">Chr13: 73890473-73893510</td><td valign="top" align="center" rowspan="1" colspan="1">969</td><td valign="top" align="center" rowspan="1" colspan="1">322</td><td valign="top" align="center" rowspan="1" colspan="1">36.45</td><td valign="top" align="center" rowspan="1" colspan="1">7</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaEF1Bγ1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_17724</td><td valign="top" align="center" rowspan="1" colspan="1">Chr06: 28533801-28535983</td><td valign="top" align="center" rowspan="1" colspan="1">1263</td><td valign="top" align="center" rowspan="1" colspan="1">420</td><td valign="top" align="center" rowspan="1" colspan="1">47.65</td><td valign="top" align="center" rowspan="1" colspan="1">7.53</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaEF1Bγ2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_17725</td><td valign="top" align="center" rowspan="1" colspan="1">Chr06: 28612381-28614486</td><td valign="top" align="center" rowspan="1" colspan="1">1179</td><td valign="top" align="center" rowspan="1" colspan="1">392</td><td valign="top" align="center" rowspan="1" colspan="1">44.63</td><td valign="top" align="center" rowspan="1" colspan="1">6.22</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaDHAR1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_30812</td><td valign="top" align="center" rowspan="1" colspan="1">Chr01: 130018051-130020359</td><td valign="top" align="center" rowspan="1" colspan="1">789</td><td valign="top" align="center" rowspan="1" colspan="1">262</td><td valign="top" align="center" rowspan="1" colspan="1">29.32</td><td valign="top" align="center" rowspan="1" colspan="1">7.67</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroplast</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaDHAR2</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_15148</td><td valign="top" align="center" rowspan="1" colspan="1">Chr07: 100493251-100495337</td><td valign="top" align="center" rowspan="1" colspan="1">639</td><td valign="top" align="center" rowspan="1" colspan="1">212</td><td valign="top" align="center" rowspan="1" colspan="1">23.44</td><td valign="top" align="center" rowspan="1" colspan="1">6.39</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaDHAR3</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_15919</td><td valign="top" align="center" rowspan="1" colspan="1">Chr12: 9370070-9371802</td><td valign="top" align="center" rowspan="1" colspan="1">639</td><td valign="top" align="center" rowspan="1" colspan="1">212</td><td valign="top" align="center" rowspan="1" colspan="1">23.50</td><td valign="top" align="center" rowspan="1" colspan="1">7.69</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoplasmic</td><td valign="top" align="left" rowspan="1" colspan="1">Plus</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaTCHQD1</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Cotton_A_36105</td><td valign="top" align="center" rowspan="1" colspan="1">Chr08: 121004224-121005417</td><td valign="top" align="center" rowspan="1" colspan="1">831</td><td valign="top" align="center" rowspan="1" colspan="1">276</td><td valign="top" align="center" rowspan="1" colspan="1">32.16</td><td valign="top" align="center" rowspan="1" colspan="1">9.05</td><td valign="top" align="left" rowspan="1" colspan="1">Nuclear</td><td valign="top" align="left" rowspan="1" colspan="1">Minus</td></tr></tbody></table></table-wrap><p>In addition to full-length <italic>GST</italic> genes, 16 partial <italic>GST</italic> genes and 4 other <italic>GST</italic> genes belong to two other subfamilies (2 of mPGES2 subfamily and 2 of C_omega_like subfamily) that distinct from the canonical GST were identified in <italic>G. raimondii</italic> genome (Supplementary Table <xref ref-type="supplementary-material" rid="SM5">2</xref>). The <italic>G. arboreum</italic> genome also contains 12 partial GST fragments and one mPGES2 and two C_omega_like genes respectively (Supplementary Table <xref ref-type="supplementary-material" rid="SM4">1</xref>). Domain structure analyses revealed that these partial <italic>GST</italic> genes contained only GST N- or C- domain or both of partial domains. Due to their small size, we were unable to analyze them in the subsequent research.</p><p>To reveal the classes of <italic>G. raimondii</italic> GSTs and <italic>G. arboreum</italic> GSTs, all these full-length GST protein sequences were initially subjected to National Center for Biotechnology Information's (NCBI) Conserved Domain Database (Marchler et al., <xref rid="B41" ref-type="bibr">2014</xref>). Results shown that all the putative GSTs of the two cotton species can be divided into eight subgroups as Tau, Phi, Theta, Zeta, Lambda, EF1Bγ, DHAR, and TCHQD. According to the proposed nomenclature for <italic>GST</italic> genes (Dixon et al., <xref rid="B11" ref-type="bibr">2002</xref>; Dixon and Edwards, <xref rid="B10" ref-type="bibr">2010</xref>), all these <italic>GST</italic> genes were designated as <italic>GrGSTs</italic> for <italic>G. raimondii</italic> and <italic>GaGSTs</italic> for <italic>G. arboreum</italic>. The genes of subgroups belong to Tau, Phi, Theta, Zeta, Lambda, EF1Bγ, DHAR, and TCHQD were named as <italic>GSTU, GSTF, GSTT, GSTZ, GSTL, EF1B</italic>γ, <italic>DHAR</italic>, and <italic>TCHQD</italic>, respectively, followed by a gene number. The numbering of each subgroup <italic>GST</italic> genes was based on their position from top to the bottom on each corresponding chromosome and different chromosomes from chromosome 1 to chromosome 13. Though the <italic>G. arboreum</italic> genome was almost two times larger than the <italic>G. raimondii</italic> (Paterson et al., <xref rid="B47" ref-type="bibr">2012</xref>; Wang et al., <xref rid="B65" ref-type="bibr">2012</xref>; Li et al., <xref rid="B33" ref-type="bibr">2014</xref>), there were only 49 <italic>GST</italic> genes identified from <italic>G. arboreum</italic>, 10 genes less than that of the <italic>G. raimondii</italic>. The length, molecular weight (Mw), isoelectric points (pI), and the predicted subcellular localization of the 59 <italic>GrGSTs</italic> and 49 <italic>GaGSTs</italic> were deduced from their predicted protein sequences. For <italic>G. raimondii</italic>, the amino acid numbers encoded from the identified <italic>GST</italic> genes varied from 194 of GrGSTU24 to 421 of GrEF1Bγ1 and GrEF1Bγ2, and their molecular weight ranged between 22.25 kDa of GrGSTU17 to 47.69 kDa of GrEF1Bγ1 and GrEF1Bγ2. Similarly, the molecular weight of GaGST proteins ranged from 15.40 kDa of GaGSTU4 to 47.65 kDa of GaEF1Bγ1, and the amino acid numbers varied from 131 of GaGSTU4 to 420 of GaEF1Bγ1. Protein subcellular localization is important for understanding its function (Chou and Shen, <xref rid="B8" ref-type="bibr">2007</xref>). Most GrGUSTs and GaGSTs were predicted to be located in the cytoplasm, only a small parts were predicted to be in the mitochondria, chloroplast, or nuclear.</p></sec><sec><title>Phylogenetic analysis of the <italic>GST</italic> gene family</title><p>To detect the phylogenetic relationship between <italic>GST</italic> genes, all the putative GSTs from two cotton species, as well as the GST proteins from Arabidopsis and rice, were aligned to generate an unrooted phylogenetic tree separately with Neiboring-Joining method (Figures <xref ref-type="fig" rid="F1">1</xref>, <xref ref-type="fig" rid="F2">2</xref>). Meanwhile, the phylogenetic trees reconstructed with Minimum Evolution method were almost identical with only minor differences at some branches (Supplementary Figures <xref ref-type="supplementary-material" rid="SM1">1</xref>, <xref ref-type="supplementary-material" rid="SM2">2</xref>), suggesting that the two methods were largely consistent with each other. The phylogenetic trees shown that GST proteins from <italic>G. raimondii</italic> or <italic>G. arboreum, Arabidopsis</italic>, and rice belonging to the same class were clustered together. It suggested that both the <italic>GST</italic> gene family of the two cotton species can be grouped into eight classes. The phylogenetic classification completely matched the classification based on NCBI CDD. It could be shown in Figure <xref ref-type="fig" rid="F1">1</xref> that Tau contained the largest number of <italic>GrGST</italic> genes (38) followed by Phi (7). This phenomenon was correspond to <italic>GST</italic> genes in other plant species (Sappl et al., <xref rid="B53" ref-type="bibr">2009</xref>; Jain et al., <xref rid="B27" ref-type="bibr">2010</xref>; Chi et al., <xref rid="B6" ref-type="bibr">2011</xref>). The plant specific Tau and Phi <italic>GSTs</italic> were inducible in plants when they were exposure to biotic and abiotic stresses (Nutricati et al., <xref rid="B44" ref-type="bibr">2006</xref>). Other two plant specific GSTs classes, Lambda and DHAR were the only GSTs shown to be active as monomers (Mohsenzadeh et al., <xref rid="B43" ref-type="bibr">2011</xref>). Theta class has a putative role in detoxifying oxidized lipids (Wagner et al., <xref rid="B64" ref-type="bibr">2002</xref>). <italic>G. raimondii</italic> had three members in each of them. Among the four representative plant species, only rice lack the Lambda GSTs. There were two <italic>GrGST</italic> genes each in Zeta and EF1Bγ class, which functions in tyrosine catabolism and the encoding of γ subunit of eukaryotic translation elongation factor. As with the unusual class of <italic>GST</italic> gene family, TCHQD, only one member existed in <italic>G. raimondii, Arabidopsis</italic>, and rice. All the <italic>GrGSTs</italic> clustered with their <italic>Arabidopsis</italic> and rice counterparts. It suggested that the <italic>GrGST</italic> genes duplicated after the divergence of <italic>G. raimondii, Arabidopsis</italic>, and rice.</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Phylogenetic relationships of <italic>GST</italic> genes from <italic>G. raimondii</italic>, <italic>Arabidopsis</italic>, and rice</bold>. The unrooted phylogentic tree was constructed using MEGA 5.2 by Neighbor-Joining method and the bootstrap test was performed with 1000 replicates. Percentage bootstrap scores of >50% were displayed. The <italic>GST</italic> genes from <italic>G. raimondii, Arabidopsis</italic> and rice were marked with the red dots, green triangles, and blue rhombuses respectively. And the branches of each subfamily were indicated in a specific color.</p></caption><graphic xlink:href="fpls-07-00139-g0001"></graphic></fig><fig id="F2" position="float"><label>Figure 2</label><caption><p><bold>Phylogenetic relationships of <italic>GST</italic> genes from <italic>G. arboreum</italic>, <italic>Arabidopsis</italic>, and rice</bold>. The unrooted phylogentic tree was constructed using MEGA 5.2 by Neighbor-Joining method and the bootstrap test was performed with 1000 replicates. Percentage bootstrap scores of >50% were displayed. The <italic>GST</italic> genes from <italic>G. arboreum, Arabidopsis</italic> and rice were marked with the red dots, green triangles, and blue rhombuses, respectively. And the branches of each subfamily were indicated in a specific color.</p></caption><graphic xlink:href="fpls-07-00139-g0002"></graphic></fig><p>Similarly, 49 <italic>GaGSTs</italic> can be grouped into the eight classes (Figure <xref ref-type="fig" rid="F2">2</xref>), Tau had the largest number of GST genes (29), followed by Phi (6). There were three GST genes each in Lambda, DHAR, and Theta, two each in Zeta and EF1Bγ, and one in TCHQD.</p></sec><sec><title>Orthologous relationships between <italic>GrGSTs</italic> and <italic>GaGSTs</italic></title><p>In order to reveal the orthologous relationships among the members of <italic>GST</italic> gene family between <italic>G. raimondii</italic> and <italic>G. arboreum</italic>, the protein sequences of 59 predicted full-length <italic>GrGST</italic> genes and 49 predicted full-length <italic>GaGST</italic> genes were further applied to construct a separate unrooted phylogenetic tree (Figure <xref ref-type="fig" rid="F3">3A</xref>). The topology of the tree indicated that there were 38 pairs of orthologous genes between <italic>G. raimondii</italic> and <italic>G. arboreum</italic>, since these <italic>GST</italic> genes from the two cotton species respectively were in the terminal branches with high bootstrap values. However, the others were divergent apparently, the orthologous relationships among them could not be confirmed. Among the most abundant Tau class in <italic>G. raimondii</italic> and <italic>G. arboreum</italic>, only 20 orthologous gene pairs were found. Whereas, Phi class harbored 6 pairs of orthologous genes apart from <italic>GrGSTF7</italic>. All the <italic>GST</italic> genes in DHAR (3 pairs), Lambda (3 pairs), Zeta (2 pairs), Theta (3 pairs), and TCHQD (1 pair) were in the adjacent clades separately, suggesting that all of them in each class were orthologous genes. The orthologous relationships between the two <italic>Gossypium</italic> species were displayed in Supplementary Figure <xref ref-type="supplementary-material" rid="SM3">3</xref>. However, all the EF1Bγ genes were of paralogous. Moreover, there were several pairs of paralogous genes in the Tau subfamily both in <italic>G. raimondii</italic> and <italic>G. arboreum</italic>, since the genes from the same genome were in the terminal branches of the phylogenetic tree.</p><fig id="F3" position="float"><label>Figure 3</label><caption><p><bold>Phylogenetic relationships and gene structure of <italic>GST</italic> genes from <italic>G. raimondii</italic> and <italic>G. arboreum</italic></bold>. <bold>(A)</bold> The phylogenetic tree of all <italic>GST</italic> genes in <italic>G. raimondii</italic> and <italic>G. arboreum</italic> was constructed using MEGA 5.2 by Neighbor-Joining method and the bootstrap test was performed with 1000 replicates. Percentage bootstrap scores of >50% were displayed. The <italic>GST</italic> genes from <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were marked with red dots and blue dots, respectively. Gene names in gray background shown orthologous pairs. <bold>(B)</bold> The exon-inton structure of <italic>GST</italic> genes from <italic>G. raimondii</italic> and <italic>G. arboreum</italic>. Exons were represented by green boxes and introns by gray lines.</p></caption><graphic xlink:href="fpls-07-00139-g0003"></graphic></fig></sec><sec><title>Gene structure of <italic>GrGSTs</italic> and <italic>GaGSTs</italic></title><p>To investigate the possible structural evolution of <italic>GST</italic> gene family in the two diploid cotton species, the gene structures of <italic>GrGSTs</italic> and <italic>GaGSTs</italic> were compared separately. The details of the comparison were illustrated in Figure <xref ref-type="fig" rid="F3">3B</xref>. In general, the exon/intron organizations of <italic>GSTs</italic> were consistent with the phylogenetic subfamilies showed in Figure <xref ref-type="fig" rid="F3">3A</xref>. And the gene structures were conserved within the same group. As an example, a host of <italic>GST</italic> genes in Tau possessed one intron, except for <italic>GaGSTU12</italic>, which contained five introns. Most members of Phi class had two introns, except for <italic>GrGSTF7</italic> which had three introns. All the members in Theta class possessed six introns except <italic>GrGST1</italic> that had seven. The structures of the genes in DHAR, TCHQD, and EF1Bγ classes were relatively highly conserved, and every gene in the same group had the same intron number. In contrast, the exon/intron distribution patterns in the genes of Lambda class were various. The intron numbers ranged from seven of <italic>GaGSTL1</italic> to nine of <italic>GaGSTL2</italic> and <italic>GrGSTL2</italic>. Zeta class also displayed great variability in gene structures. <italic>GaGSTZ2</italic> had 13 introns, which is the maximum in all the <italic>GST</italic> genes, and <italic>GrGSTZ1</italic> contained nine introns, while <italic>GrGSTZ2</italic> and <italic>GaGSTZ1</italic> each had eight introns. As expected, the gene structures of orthologous pairs were almost identical with only minor differences with the exception of <italic>GrGSTU22</italic>/<italic>GaGSTU4, GrGSTU17</italic>/<italic>GaGSTU16, GrGSTL1</italic>/<italic>GaGSTL1, GrGSTZ1</italic>/<italic>GaGSTZ1</italic>, and <italic>GrGSTT1</italic>/<italic>GaGSTT1</italic>. Additionally, the gene structures among the orthologous pairs were uniformly observed in Phi and EF1Bγ classes.</p></sec><sec><title>Chromosomal localization and gene duplication</title><p>The 59 non-redundant <italic>GrGST</italic> genes were mapped on the 13 <italic>G. raimondii</italic> chromosomes (Figure <xref ref-type="fig" rid="F4">4</xref>). Normally, the number of <italic>GrGST</italic> genes on each chromosome varied widely. Chromosome 13 contained 10 <italic>GST</italic> genes, followed by chromosome 7 and chromosome 5 on which nine and eight members were found, respectively. Chromosome 12 had six genes, and chromosome eight had five. Chromosome 4, Chromosome 6, and Chromosome 11 contained four genes each. There were three <italic>GST</italic> genes on Chromosome 1. Both chromosome 2 and chromosome 3 harbored two genes, whereas each only single <italic>GST</italic> gene was localized on chromosome 9 and chromosome 10. Obviously, they were distributed unevenly among 13 chromosomes. In addition, most of the <italic>GrGST</italic> genes in Tau class were clustered on chromosomes. Referred to the criterion of tandem duplication (Zhao et al., <xref rid="B70" ref-type="bibr">2014</xref>; Qiao et al., <xref rid="B48" ref-type="bibr">2015</xref>), we defined gene cluster as that two adjacent <italic>GST</italic> genes were separated by a maximum of five intervening genes. A total of seven gene clusters were detected on seven different chromosomes, and six of them were from tau class (22 genes) and the other was produced by the genes that from EF1Bγ class (two genes). It had been revealed that tandem duplication and/or segmental duplication played a significant role in the generation of gene families. To elucidate the expanded mechanism of <italic>GST</italic> gene family in <italic>G. raimondii</italic>, the gene duplication events were investigated, and 12 tandem duplication events, <italic>GrGSTU5</italic>/<italic>GrGSTU6, GrGSTU7</italic>/<italic>GrGSTU11, GrGSTU8</italic>/<italic>GrGSTU7, GrGSTU9</italic>/<italic>GrGSTU8, GrGSTU10</italic>/ <italic>GrGSTU12, GrGSTU12</italic>/<italic>GrGSTU13, GrGSTU13</italic>/<italic>GrGSTU10, GrGSTU28</italic>/<italic>GrGSTU29, GrGSTU35</italic>/<italic>GrGSTU36, GrGSTU36</italic>/<italic>GrGSTU37, GrGSTU37</italic>/<italic>GrGSTU35</italic>, and <italic>GrEF1B</italic>γ<italic>1</italic>/<italic>GrEF1B</italic>γ<italic>2</italic>, were detected in the <italic>G. raimondii</italic> genome (Figure <xref ref-type="fig" rid="F4">4</xref>). Interestingly, all tandem duplicated gene pairs were concluded in their different gene clusters respectively. Furthermore, three segmental duplication events, <italic>GrGSTU21</italic>/<italic>GrGSTU26, GrGSTU24</italic>/<italic>GrGSTU32</italic>, and <italic>GrDHAR2</italic>/<italic>GrDHAR3</italic>, were detected. It suggested that both the two kinds of duplication events contributed to the <italic>GST</italic> gene family expansion in <italic>G. raimondii</italic>.</p><fig id="F4" position="float"><label>Figure 4</label><caption><p><bold>Chromosomal distribution and gene duplication of <italic>GST</italic> genes in <italic>G. raimondii</italic></bold>. The chromosome number was indicated at the top of each chromosome representation. The scale on the left was in megabases (Mb). The genes with a pentagram left represent <italic>GST</italic> gene clusters. The tandem duplicated genes were highlighted with outlined boxes. And the segmental duplicated gene pairs are connected with red lines.</p></caption><graphic xlink:href="fpls-07-00139-g0004"></graphic></fig><p>Like the case in <italic>G. raimondii</italic>, the 49 <italic>GaGST</italic> gene loci distributed unevenly across the 13 chromosomes in <italic>G. arboreum</italic>, ranging from 1 to 8 genes per chromosome (Figure <xref ref-type="fig" rid="F5">5</xref>). A maximum number of eight genes were located on chromosome 13 closely, followed by seven genes on chromosome 11. In contrast, only one gene was located on chromosome 2 and chromosome 9 each. There were also seven gene clusters distributed on seven different chromosomes. Analogously, six out of the seven gene clusters were composed of 19 <italic>GaGSTs</italic> in Tau class and the rest one was formed by <italic>GaEF1B</italic>γ class. A total of 10 tandem duplication events and one segmental duplication event were found. We also concluded that the expansion of <italic>GST</italic> gene family in <italic>G. arboreum</italic> was mainly attributed to tandem duplication events rather than segmental duplication event.</p><fig id="F5" position="float"><label>Figure 5</label><caption><p><bold>Chromosomal distribution and gene duplication of <italic>GST</italic> genes in <italic>G. arboreum</italic></bold>. The chromosome number was indicated at the top of each chromosome representation. The scale on the left was in megabases (Mb). The genes with a pentagram left represent <italic>GST</italic> gene clusters. Red outlined boxes represent tandem duplicated genes. And the segmental duplicated gene pairs were connected with red lines.</p></caption><graphic xlink:href="fpls-07-00139-g0005"></graphic></fig></sec><sec><title>Selective pressure analysis of the duplicated <italic>GST</italic> genes</title><p>To investigate the selective constrains on duplicated <italic>GST</italic> genes, the non-synonymous to synonymous substitution ratio (Ka/Ks) for each pair of duplicated <italic>GST</italic> genes were calculated. Generally, Ka/Ks ratio >1 indicates positive selection, Ka/Ks = 1 indicates neutral selection, while a ratio < 1 indicates negative or purifying selection. In this study, 15 duplicated pairs in the <italic>G. raimondii</italic> and 11 duplicated pairs in <italic>G. arboreum GST</italic> gene family were investigated respectively. In <italic>G. raimondii</italic>, the Ka/Ks ratio for 11 duplicated pairs were < 1 (Table <xref ref-type="table" rid="T3">3</xref>), with most of them being even < 0.3, which suggested that they had experienced strong purifying selection pressure. However, the remaining four duplicated pairs with ratios >1 seemed to be under positive selection. While in the case of <italic>G. arboreum</italic>, 10 out of 11 duplicated pairs had undergone purifying selection pressure, and only one pair of duplicated <italic>GST</italic> genes with a ratio >1 were found in <italic>G. arboreum</italic>. Those observations reflected that the functions of the duplicated <italic>GST</italic> genes in the two cottons did not diverge much during subsequent evolution. And the purifying selection might contribute largely to the maintenance of function in <italic>G. arboreum</italic> GST family.</p><table-wrap id="T3" position="float"><label>Table 3</label><caption><p><bold>Ka/Ks analysis for the duplicated <italic>GST</italic> gene pairs from <italic>G. raimondii</italic> and <italic>G. arboretum</italic></bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Species</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Duplicated gene 1</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Duplicated gene 2</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Ka</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Ks</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Ka/Ks</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Purifying selection</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Duplicate type</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>G. raimondii</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU5</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU6</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.016</td><td valign="top" align="center" rowspan="1" colspan="1">0.036</td><td valign="top" align="center" rowspan="1" colspan="1">0.451</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU7</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU11</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.126</td><td valign="top" align="center" rowspan="1" colspan="1">0.463</td><td valign="top" align="center" rowspan="1" colspan="1">0.271</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU8</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU7</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.102</td><td valign="top" align="center" rowspan="1" colspan="1">0.380</td><td valign="top" align="center" rowspan="1" colspan="1">0.269</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU9</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU8</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.043</td><td valign="top" align="center" rowspan="1" colspan="1">0.305</td><td valign="top" align="center" rowspan="1" colspan="1">0.142</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU10</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU12</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.042</td><td valign="top" align="center" rowspan="1" colspan="1">0.083</td><td valign="top" align="center" rowspan="1" colspan="1">0.513</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU12</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU13</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.100</td><td valign="top" align="center" rowspan="1" colspan="1">0.293</td><td valign="top" align="center" rowspan="1" colspan="1">0.340</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU13</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU10</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.083</td><td valign="top" align="center" rowspan="1" colspan="1">0.023</td><td valign="top" align="center" rowspan="1" colspan="1">3.544</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU21</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU26</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.016</td><td valign="top" align="center" rowspan="1" colspan="1">0.007</td><td valign="top" align="center" rowspan="1" colspan="1">2.275</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Segmental</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU24</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU32</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.054</td><td valign="top" align="center" rowspan="1" colspan="1">0.044</td><td valign="top" align="center" rowspan="1" colspan="1">1.227</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Segmental</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU28</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU29</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.009</td><td valign="top" align="center" rowspan="1" colspan="1">0.019</td><td valign="top" align="center" rowspan="1" colspan="1">0.489</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU35</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU36</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.020</td><td valign="top" align="center" rowspan="1" colspan="1">0.015</td><td valign="top" align="center" rowspan="1" colspan="1">1.361</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU36</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU37</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.085</td><td valign="top" align="center" rowspan="1" colspan="1">0.290</td><td valign="top" align="center" rowspan="1" colspan="1">0.291</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU37</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrGSTU35</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.080</td><td valign="top" align="center" rowspan="1" colspan="1">0.292</td><td valign="top" align="center" rowspan="1" colspan="1">0.276</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrDHAR2</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrDHAR3</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.084</td><td valign="top" align="center" rowspan="1" colspan="1">0.501</td><td valign="top" align="center" rowspan="1" colspan="1">0.168</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Segmental</td></tr><tr style="border-bottom: thin solid #000000;"><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrEF1Bγ1</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GrEF1Bγ2</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.004</td><td valign="top" align="center" rowspan="1" colspan="1">0.022</td><td valign="top" align="center" rowspan="1" colspan="1">0.187</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>G. arboreum</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU5</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU6</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.121</td><td valign="top" align="center" rowspan="1" colspan="1">0.463</td><td valign="top" align="center" rowspan="1" colspan="1">0.261</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU6</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU7</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.064</td><td valign="top" align="center" rowspan="1" colspan="1">0.421</td><td valign="top" align="center" rowspan="1" colspan="1">0.153</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU8</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU9</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.059</td><td valign="top" align="center" rowspan="1" colspan="1">0.097</td><td valign="top" align="center" rowspan="1" colspan="1">0.615</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU13</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU14</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.071</td><td valign="top" align="center" rowspan="1" colspan="1">0.164</td><td valign="top" align="center" rowspan="1" colspan="1">0.431</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU14</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU15</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.065</td><td valign="top" align="center" rowspan="1" colspan="1">0.187</td><td valign="top" align="center" rowspan="1" colspan="1">0.350</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU15</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU13</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.048</td><td valign="top" align="center" rowspan="1" colspan="1">0.170</td><td valign="top" align="center" rowspan="1" colspan="1">0.280</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU24</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU25</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.015</td><td valign="top" align="center" rowspan="1" colspan="1">0.009</td><td valign="top" align="center" rowspan="1" colspan="1">1.591</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU25</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU26</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.082</td><td valign="top" align="center" rowspan="1" colspan="1">0.328</td><td valign="top" align="center" rowspan="1" colspan="1">0.251</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU26</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaGSTU24</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.098</td><td valign="top" align="center" rowspan="1" colspan="1">0.308</td><td valign="top" align="center" rowspan="1" colspan="1">0.316</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaDHAR2</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaDHAR3</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.077</td><td valign="top" align="center" rowspan="1" colspan="1">0.462</td><td valign="top" align="center" rowspan="1" colspan="1">0.166</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Segmental</td></tr><tr><td rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaEF1Bγ1</italic></td><td valign="top" align="left" rowspan="1" colspan="1"><italic>GaEF1Bγ2</italic></td><td valign="top" align="center" rowspan="1" colspan="1">0.008</td><td valign="top" align="center" rowspan="1" colspan="1">0.040</td><td valign="top" align="center" rowspan="1" colspan="1">0.194</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Tandem</td></tr></tbody></table></table-wrap></sec><sec><title>The expression profiles of potential salt stress-responsive <italic>GST</italic> genes</title><p>Salt stress is one of the serious environmental stresses that most land plants might encounter during the process of their growth. Many GSTs have been implicated in various abiotic stress responses in plants (Droog, <xref rid="B13" ref-type="bibr">1997</xref>; Scarponi et al., <xref rid="B54" ref-type="bibr">2006</xref>; Sharma et al., <xref rid="B56" ref-type="bibr">2014</xref>; Yang et al., <xref rid="B67" ref-type="bibr">2014</xref>). However, little is known about the functions of <italic>GST</italic> genes in the cotton response to salt stress. The <italic>cis</italic>-elements in gene promoter regions might provide some indirect evidence for the functional dissection of <italic>GST</italic> genes in stress response (Zhou et al., <xref rid="B71" ref-type="bibr">2013</xref>). Though the specific items of salt-responsive element were not existed in the PLACE database, some <italic>cis</italic>-elements might respond to multiple environment stimuli (Higo et al., <xref rid="B25" ref-type="bibr">1999</xref>). All of putative environment stimulus responsive <italic>cis</italic>-elements in cotton <italic>GST</italic> genes were detected (Supplementary Table <xref ref-type="supplementary-material" rid="SM6">3</xref>). The results revealed that the majority of <italic>GST</italic> genes, 19 <italic>GrGSTs</italic>, and 21 <italic>GaGSTs</italic>, contained relevant <italic>cis</italic>-elements in promoter sequences, which indicated that these cotton GST genes might the signal transduction of the plant response to salt stress.</p><p>To verify the expression patterns of these <italic>GST</italic> genes, a comprehensive qRT-PCR analysis of 40 selected <italic>GSTs</italic> were performed (Figure <xref ref-type="fig" rid="F6">6</xref>). As shown in Figure <xref ref-type="fig" rid="F6">6</xref>, cotyledons and leaves exhibited more concentrated expression levels compared with roots and stems. Most of these 40 cotton <italic>GST</italic> genes had specific spatial expression patterns. <italic>GrDHAR2, GaGSTU15, GaGSTF3</italic>, and <italic>GaGSTU14</italic> preferentially expressed both in cotyledons and leaves, and <italic>GrGSTZ2</italic> were highly expressed in all tissues detected. There were seven orthologs among the selected genes, but only one pair <italic>GrGSTU30</italic>/<italic>GaGSTU20</italic> clustered together. It was inferred that the expression of <italic>GST</italic> orthologs between <italic>G. raimondii</italic> and <italic>G. arboreum</italic> have experienced divergence.</p><fig id="F6" position="float"><label>Figure 6</label><caption><p><bold>Expression patterns of 40 selected <italic>GST</italic> genes in four representative tissues of <italic>G. raimondii</italic> and <italic>G. arboreum</italic></bold>. The color bar represents the relative signal intensity values.</p></caption><graphic xlink:href="fpls-07-00139-g0006"></graphic></fig><p>The expression of all the selected <italic>GST</italic> genes has also been conducted in the roots, stems, cotyledons and leaves of two cotton species under salt treatments. Results showed altered expression patterns of either induction or suppression associated with at least one salt concentration (Figure <xref ref-type="fig" rid="F7">7</xref>). In roots, nearly all the selected <italic>GST</italic> genes showed up-regulated expression after salt treatment except for <italic>GaGSTF6</italic> and <italic>GaGSTU20</italic>. In stems, <italic>GaGSTF1, GaDHAR1, GaGSTU24, GaGSTF2</italic>, and <italic>GrGSTU30</italic> were down-regulated. Several <italic>GST</italic> genes displayed initial up-regulation and subsequent down-regulation. However, only a few up-regulated expressed <italic>GST</italic> genes were found in cotyledons compared with roots. <italic>GaGSTF1, GaGSTU29, GaGSTU7</italic>, and <italic>GrEF1B</italic>γ<italic>1</italic> showed insignificantly up-regulated expression by salt inducing in cotyledons. In leaves, the expressions of most selected <italic>GST</italic> genes were up-regulated just under slight salt stress. Nevertheless, <italic>GaGSTU29, GrGSTU16, GaGSTZ1</italic>, and <italic>GrGSTF4</italic> showed continued up-regulation in different level of salt stress. In addition, only one orthologs, <italic>GaGSTF2</italic>/<italic>GrGSTF2</italic>, were clustered together with similar expression patterns.</p><fig id="F7" position="float"><label>Figure 7</label><caption><p><bold>Expression patterns of 40 selected <italic>GST</italic> genes in four representative tissues of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> under salt stress</bold>. The color bar represents the relative signal intensity values. The slight stress, moderate stress, and severe stress represent 50, 100, and 200 mM NaCl in <italic>G. raimondii</italic> and 100, 200, and 300 mM NaCl in <italic>G. arboreum</italic>, respectively.</p></caption><graphic xlink:href="fpls-07-00139-g0007"></graphic></fig></sec></sec><sec sec-type="discussion" id="s4"><title>Discussion</title><p>Salinity resulting mainly from NaCl is one of common environmental stresses that afflict the growth and yield of crops in many places of the world (Shabala, <xref rid="B55" ref-type="bibr">2013</xref>). Salt stress may increase the reactive oxygen species (ROS) and damage the integrity of cell membranes, which triggering the disturbance of metabolism (Zhu, <xref rid="B72" ref-type="bibr">2002</xref>). Plant adaptation to salt stress involved a series of biochemical pathways and lots of active compounds such as antioxidant enzymes (Guo et al., <xref rid="B23" ref-type="bibr">2001</xref>).</p><sec><title>Phylogenetic analyses and evolution of <italic>GST</italic> gene family in <italic>G. raimondii</italic> and <italic>G. arboreum</italic></title><p>A growing numbers of research works were devoted to elucidating the roles of plant GSTs in growth and stress responses (Oakley, <xref rid="B45" ref-type="bibr">2005</xref>; Dixon et al., <xref rid="B12" ref-type="bibr">2010</xref>; Skopelitou et al., <xref rid="B58" ref-type="bibr">2012</xref>). A total of 59 and 49 putative <italic>GST</italic> genes were identified in the genomes of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> respectively in present work. Phylogenetic analyses revealed that both <italic>GrGSTs</italic> and <italic>GaGSTs</italic> were more closely allied to <italic>AtGSTs</italic> than to <italic>OsGSTs</italic>, which were consistent with the evolutionary relationships among <italic>G. raimondii, G. arboreum, Arabidopsis</italic>, and rice. Moreover, all the <italic>GST</italic> genes from the three representative dicot species sorted into eight distinct clades, except the Lambda class which was absent in rice. This implied that these seven subfamilies but Lambda arose before divergence the monocots-dicots. In turns, Lambda group was either acquired after the evolutionary split of monocots-dicots or lost in rice. Intriguingly, the member of <italic>GST</italic> gene family in <italic>G. raimondii</italic> was a little bit more than that in <italic>Arabidopsis</italic> (55) and much less than that in rice (77). It was more obvious in the case of <italic>G. arboreum</italic> which contained the minimum <italic>GST</italic> genes among the four representative species, albeit the genomes of the two diploid cottons were larger than that of <italic>Arabidopsis</italic> and rice. A proper explanation of the phenomenon was that the transposable elements represented a major component of <italic>Gossypium</italic> genome (Hawkins et al., <xref rid="B24" ref-type="bibr">2006</xref>).</p></sec><sec><title>Tandem duplication plays a major role in the expansion of <italic>GST</italic> gene family in <italic>G. raimondii</italic> and <italic>G. arboreum</italic></title><p>Like the <italic>GST</italic> gene families in other known plants (Soranzo et al., <xref rid="B59" ref-type="bibr">2004</xref>; Sappl et al., <xref rid="B53" ref-type="bibr">2009</xref>), most <italic>GST</italic> gene loci in <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were present in genomes in clusters of two to seven genes. There were seven gene clusters each in the genomes of <italic>G. raimondii</italic> and <italic>G. arboreum</italic>, presumably as a result of multiple tandem duplication events in the common ancestor of <italic>Gossypium</italic>. The classifications of full-length <italic>GST</italic> genes suggested that whether in <italic>G. raimondii</italic> or <italic>G. arboreum</italic>, the members of Tau <italic>GSTs</italic> and Phi <italic>GSTs</italic> were more than the others. In addition, Tau <italic>GSTs</italic> occupied 12 of the total 14 <italic>GST</italic> gene clusters in the two diploid cottons. The rest of them were composed of EF1Bγ <italic>GSTs</italic>. It has been demonstrated that the expansion of gene families is mainly caused by gene duplication events, including tandem duplication, segmental duplication, transposition events, and whole-genome duplication (Blanc and Wolfe, <xref rid="B3" ref-type="bibr">2004</xref>; Flagel and Wendel, <xref rid="B18" ref-type="bibr">2009</xref>). It also could be speculated that the amplification of the <italic>GST</italic> gene family were mainly caused by the tandem duplication for Tau and Phi classes both in <italic>G. raimondii</italic> and <italic>G. arboreum</italic>. An intriguing finding was that purifying selection has predominated across the duplicated genes. The reasons might be that (1) deleterious mutations might occur in different domains in copies of genes with multiple independent domain subfunctions (Force et al., <xref rid="B19" ref-type="bibr">1999</xref>; Lan et al., <xref rid="B30" ref-type="bibr">2009</xref>); (2) purifying selection could eliminate deleterious loss-of-function mutations, thus fixed a new duplicate gene and enhanced the preservation of functional alleles at both duplicate loci (Tanaka et al., <xref rid="B61" ref-type="bibr">2009</xref>). In addition, the number of <italic>GaGST</italic> genes was less than that of <italic>GrGSTs</italic>, although the genome size of <italic>G. arboreum</italic> is almost twice larger than that of <italic>G. raimondii</italic> (Paterson et al., <xref rid="B47" ref-type="bibr">2012</xref>; Wang et al., <xref rid="B65" ref-type="bibr">2012</xref>; Li et al., <xref rid="B33" ref-type="bibr">2014</xref>). A theoretical explanation was that <italic>G. arboreum</italic> had undergone large-scale retrotransposons insertion during evolution (Li et al., <xref rid="B33" ref-type="bibr">2014</xref>).</p></sec><sec><title>Functional divergence of specific cotton <italic>GST</italic> genes under salt stress</title><p>It is worth to notice that orthologous <italic>GST</italic> gene pairs demonstrated very similar exon/intron distribution patterns in terms of exon length and intron number. However, the expression patterns of them were divergent. It might involve with the adaptation to different habitat of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> after their species-specific evolution. Remarkably, the exons of the <italic>GST</italic> genes in the same classes were highly conserved whether of intraspecies or interspecies, but the introns were various with indel mutations (Xu et al., <xref rid="B66" ref-type="bibr">2012</xref>). Further analyses are needed to elucidate the impacts of intron variation on gene function. The gene expression patterns can provide important clues for gene function. The tissue-specific expression patterns of 40 selected <italic>GST</italic> genes under normal condition reflected that they might play versatile functions in the growth and development of cotton. Additionally, they also shown divergent expression patterns under salt treatment. It is clear that the roots are the first tissues which salt stress directly affected in the soil or culture solution (Guo et al., <xref rid="B23" ref-type="bibr">2001</xref>). In our study, what consistent with the fact proposed was that almost all the selected <italic>GST</italic> genes were up-regulated in response to salt stress in roots. By contrast, a majority of genes showed up-regulation in leaves only under slight salt stress. This was probably associated with the facts that these two tissues by themselves were distinct in structure and functions (Qing et al., <xref rid="B49" ref-type="bibr">2009</xref>; Campo et al., <xref rid="B4" ref-type="bibr">2014</xref>). Duplicate genes might have three different evolutionary fates, i.e., nonfunctionalization, subfunctionalization, and neofunctionalization (Liu et al., <xref rid="B36" ref-type="bibr">2014</xref>). The expression pattern shifts of the duplicated genes <italic>GaGSTU14</italic>/<italic>GaGSTU15</italic> indicated the functional divergence after duplicated events. Among the seven orthologs, only one pair, <italic>GrGSTF2</italic>/<italic>GaGSTF2</italic>, clustered together under salt treatment. These findings further supported the assertion that expression divergence is often the first step in the functional divergence between duplicate genes, thereby increases the chance of duplicate genes being retained in a genome (Zhang, <xref rid="B69" ref-type="bibr">2003</xref>).</p><p>In short, the <italic>GST</italic> gene family both in <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were identified and characterized using bioinformatics approaches, and the results have provided a basis for further assessment of physiological roles of different <italic>GST</italic> genes in response to salt stress in <italic>Gossypium</italic> species.</p></sec></sec><sec id="s5"><title>Author contributions</title><p>YD, SZ, and JC conceived all the experiments and analyzed data. YD performed experiments, drafted the manuscript and prepared the figures. YD and SZ wrote and reviewed the manuscript. CL and YZ prepared figures. QH analyzed data. JC performed the experiments. MD contributed to the manuscript preparation. All authors reviewed the manuscript.</p><sec><title>Conflict of interest statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer SR and Handling Editor declared their shared affiliation, and the Handling Editor states that the process nevertheless met the standards of a fair and objective review.</p></sec></sec></body><back><ack><p>We are grateful to Wei Li, Wei Liu, Li Chen, Lu Zhang, Jieqiong Huang, Jiyu Feng, and Tianlun Zhao (Zhejiang University, China) for their support in this study. The work was funded by National Basic Research Program (973 program, No: 2010CB126006), and National High Technology Research and Development Program of China (2011AA10A102, 2013AA102601).</p></ack><sec sec-type="supplementary-material" id="s6"><title>Supplementary material</title><p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="http://journal.frontiersin.org/article/10.3389/fpls.2016.00139">http://journal.frontiersin.org/article/10.3389/fpls.2016.00139</ext-link></p><supplementary-material content-type="local-data" id="SM1"><label>Supplementary Figure 1</label><caption><p><bold>Phylogenetic analysis of <italic>GST</italic> genes from <italic>G. raimondii, Arabidopsis</italic>, and rice</bold>. The unrooted phylogentic tree was constructed using MEGA 5.2 by Minimum Evolution method and the bootstrap test was performed with 1000 replicates. Percentage bootstrap scores of >50% were displayed. The <italic>GST</italic> genes from <italic>G. raimondii, Arabidopsis</italic> and rice were marked with the dots, triangles, and rhombuses, respectively.</p></caption><media xlink:href="Image1.JPEG"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM2"><label>Supplementary Figure 2</label><caption><p><bold>Phylogenetic analysis of <italic>GST</italic> genes from <italic>G. arboreum, Arabidopsis</italic>, and rice</bold>. The unrooted phylogentic tree was constructed using MEGA 5.2 by Minimum Evolution method and the bootstrap test was performed with 1000 replicates. Percentage bootstrap scores of >50% were displayed. The <italic>GST</italic> genes from <italic>G. arboreum, Arabidopsis</italic> and rice were marked with the dots, triangles, and rhombuses, respectively.</p></caption><media xlink:href="Image2.JPEG"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM3"><label>Supplementary Figure 3</label><caption><p><bold>Locations and orthologs of <italic>GST</italic> genes in <italic>G. raimondii</italic> and <italic>G. arboreum</italic></bold>. The picture was generated by Circos software. The chromosomes of <italic>G. raimondii</italic> and <italic>G. arboreum</italic> were shown with different colors and labeled as Gr and Ga, respectively. The putative orthologous genes belonging to the Tau, Phi, Lambda, DHAR, Zeta, Theta, and TCHQD1 subfamilies were connected by yellow, green, blue, purple, orange, red, and gray lines, respectively.</p></caption><media xlink:href="Image3.JPEG"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM4"><label>Supplementary Table 1</label><caption><p><bold>PCR primers used in this study</bold>.</p></caption><media xlink:href="Table1.DOC"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM5"><label>Supplementary Table 2</label><caption><p><bold>The information of partial <italic>GST</italic> genes and mPGES2 and C_pmega_lke subfamilies in <italic>G. raimondii</italic> and <italic>G. arboreum</italic></bold>.</p></caption><media xlink:href="Table2.DOC"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM6"><label>Supplementary Table 3</label><caption><p><bold>The <italic>cis</italic>-elements involved in salt stress response in the promoter regions of <italic>GrGSTs</italic> and <italic>GaGSTs</italic></bold>.</p></caption><media xlink:href="Table3.DOC"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Armstrong</surname><given-names>R. 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