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Article(id=1210148022827225533, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1210148010437243088, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2022-0440, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1649779200000, receivedDateStr=2022-04-13, revisedDate=1651680000000, revisedDateStr=2022-05-05, acceptedDate=null, acceptedDateStr=null, onlineDate=1766451372105, onlineDateStr=2025-12-23, pubDate=1660233600000, pubDateStr=2022-08-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766451372105, onlineIssueDateStr=2025-12-23, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766451372105, creator=13701087609, updateTime=1766451372105, updator=13701087609, issue=Issue{id=1210148010437243088, tenantId=1146029695717560320, journalId=1189982191388893191, year='2022', volume='57', issue='8', pageStart='2245', pageEnd='2556', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1766451369151, creator=13701087609, updateTime=1766451533022, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1210148697808179705, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1210148010437243088, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1210148697808179706, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1210148010437243088, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=2528, endPage=2542, ext={EN=ArticleExt(id=1210148023280210400, articleId=1210148022827225533, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=The identification of bZIP gene family in Cannabis sativa L. and its preliminary research of the function in regulation of lipid metabolism, columnId=1190335348761793317, journalTitle=Acta Pharmaceutica Sinica, columnName=Original Articles, runingTitle=null, highlight=null, articleAbstract=

The bZIP (basic leucine zipper) gene family is one of the largest transcription factor families in eukaryotes, and its members play important roles in stress response, secondary metabolism, plant growth, seed development and other aspects. To investigate the biological functions of the bZIP (CsbZIP) gene in Cannabis sativa L., we systematically investigated the CsbZIP gene family using bioinformatics methods based on the whole-genome and transcriptome data. The results showed that 55 CsbZIP gene family members (CsbZIP1-CsbZIP55) were identified and distributed on 10 chromosomes, belonging to 12 subfamilies. The gene structure and protein motif distribution of the same subfamily members were similar. Segment repeats were the main reasons for the expansion of CsbZIP gene family. Cis-elements analysis showed that the promoter regions of 73 lipid synthesis genes contained G-box or A-box element. qRT-PCR showed that the relative expression levels of 7 CsbZIP genes and 7 lipid synthesis genes were relatively high in hemp seed. 7 CsbZIP genes had a significant positive correlation with 7 lipid synthesis genes. This study revealed the structural features, evolutionary patterns and expression patterns of CsbZIP, providing important clues for further study on the regulation of CsbZIP on oil metabolism of hemp seed.

, correspAuthors=Lin-lin DONG, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2022 Acta Pharmaceutica Sinica. All rights reserved., copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=Hao HUAI, Kang NING, Cong HOU, Shu-ming YANG, Jun-zhi WANG, Shi-lin CHEN, Lin-lin DONG), CN=ArticleExt(id=1210148027310936877, articleId=1210148022827225533, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=火麻仁基原植物bZIP基因家族鉴定及其调控油脂代谢的功能初探, columnId=1190335348896011050, journalTitle=药学学报, columnName=研究论文, runingTitle=null, highlight=null, articleAbstract=

bZIP (basic leucine zipper) 基因家族是真核生物中最大的转录因子家族之一, 其成员在逆境响应、次级代谢、植物生长、种子发育等方面发挥着重要作用。为探究火麻仁基原植物大麻(Cannabis sativa L.) bZIP (CsbZIP) 基因的生物学功能, 本研究基于大麻全基因组和转录组数据, 利用生物信息学方法对CsbZIP基因家族进行系统性研究。结果表明, 在大麻中鉴定到55个CsbZIP基因家族成员(CsbZIP1~CsbZIP55), 分布在10条染色体上, 属于12个亚家族, 同一亚家族成员之间的基因结构和蛋白基序分布相似。片段重复是CsbZIP基因家族扩张的主要因素。顺式作用元件分析表明73个油脂合成基因的启动子区含有G-box或A-box元件, qRT-PCR实验表明7个CsbZIP基因和7个油脂合成基因在火麻仁中的相对表达量较高。相关性分析表明7个CsbZIP基因和7个油脂合成基因之间存在显著的正相关关系。本研究揭示了CsbZIP基因的结构特征、进化方式和表达模式, 为进一步研究CsbZIP基因对火麻仁油脂代谢的调控提供了重要线索。

, correspAuthors=董林林, authorNote=null, correspAuthorsNote=
*董林林, E-mail:
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Int J Mol Sci, 2020, 22: 253., articleTitle=Insight into the bZIP gene family in Solanum tuberosum: genome and transcriptome analysis to understand the roles of gene diversification in spatiotemporal gene expression and function, refAbstract=null)], funds=[Fund(id=1210148037356294459, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, awardId=SQ2021PTZ0052, language=CN, fundingSource=海南省院士创新平台科研项目(SQ2021PTZ0052), fundOrder=null, country=null), Fund(id=1210148037498900800, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, awardId=2019YFC1711100, language=CN, fundingSource=国家重点研发计划资助: 中药多组学方法创新及新品种选育研究(2019YFC1711100), fundOrder=null, country=null), Fund(id=1210148037582786885, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, awardId=H2021038, language=CN, fundingSource=高品质工业大麻品种培育及开发研究(H2021038), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1210148028040745843, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, xref=null, ext=[AuthorCompanyExt(id=1210148028049134452, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, companyId=1210148028040745843, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1. 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Ltd., Kunming 650217, China), AuthorCompanyExt(id=1210148028309181325, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, companyId=1210148028292404108, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=3.云南大麻产业投资有限公司, 云南 昆明 650217)])], figs=[ArticleFig(id=1210148034609025197, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=lGV3E8AQuDQ5MU5ZY7+p2Q==, figureFileBig=zNWFdcNdKmEwwu8Yu/hJkw==, tableContent=null), ArticleFig(id=1210148034701299892, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 1, caption= Phylogenetic tree of <i>bZIP</i> genes in <i>Cannabis sativa</i> and <i>Arabidopsis thaliana</i> was constructed using MEGA7.0 based on the NJ method; bootstrap was 1 000 replicates , figureFileSmall=lGV3E8AQuDQ5MU5ZY7+p2Q==, figureFileBig=zNWFdcNdKmEwwu8Yu/hJkw==, tableContent=null), ArticleFig(id=1210148034927792319, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=PaZL5PvUcpq+YZAxolmKvw==, figureFileBig=7LMCp6J0ZHUyFYCIIJMJPA==, tableContent=null), ArticleFig(id=1210148035028455621, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 2, caption= Phylogenetic relationship, gene structure and conserved motifs of <i>bZIP</i> genes in <i>Cannabis sativa</i> , figureFileSmall=PaZL5PvUcpq+YZAxolmKvw==, figureFileBig=7LMCp6J0ZHUyFYCIIJMJPA==, tableContent=null), ArticleFig(id=1210148035133313227, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=5hqmNL/FmRz/h5RsFXFKkQ==, figureFileBig=6tbAnMhF4yNffk9OJhjwuA==, tableContent=null), ArticleFig(id=1210148035242365140, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 3, caption= Chromosomal locations of <i>CsbZIP</i> genes on <i>Cannabis sativa</i> chromosomes , figureFileSmall=5hqmNL/FmRz/h5RsFXFKkQ==, figureFileBig=6tbAnMhF4yNffk9OJhjwuA==, tableContent=null), ArticleFig(id=1210148035317862618, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=qDMYQXhiPQ9qqU1vbsCMFw==, figureFileBig=TpJaWFtdoEpY8e1+jCj6xA==, tableContent=null), ArticleFig(id=1210148035405943008, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 4, caption= Collinearity analysis of the <i>bZIP</i> gene family in <i>Cannabis sativa</i>. The gray lines indicate synteny blocks in the <i>Cannabis sativa</i> genome, while the red lines between chromosomes indicate segmental duplicated gene pairs , figureFileSmall=qDMYQXhiPQ9qqU1vbsCMFw==, figureFileBig=TpJaWFtdoEpY8e1+jCj6xA==, tableContent=null), ArticleFig(id=1210148035544355047, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=/bQqlUQhB1IxMBSR36C6mQ==, figureFileBig=OWdOmYtas2uS47E1QF+CSg==, tableContent=null), ArticleFig(id=1210148035686961387, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 5, caption= Synteny analysis of <i>bZIP</i> genes between <i>Cannabis sativa</i> and four representative plant species. Gray lines in the background indicate the collinear blocks within <i>Cannabis sativa</i> and other plant genomes, while the red lines highlight the syntenic <i>bZIP</i> gene pairs. The specie names with the prefixes '<i>C. sativa</i>', '<i>A. thaliana</i>', '<i>V. vinifera</i>', '<i>O. sativa</i>' and '<i>Z. mays</i>' indicate <i>Cannabis sativa</i>, <i>Arabidopsis thaliana</i>, <i>Vitis vinifera</i>, <i>Oryza sativa</i>, and <i>Zea mays</i>, respectively , figureFileSmall=/bQqlUQhB1IxMBSR36C6mQ==, figureFileBig=OWdOmYtas2uS47E1QF+CSg==, tableContent=null), ArticleFig(id=1210148035775041774, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=ZFTC95fvvhmij2wnTXVr9A==, figureFileBig=efkoN6f45F0RG/xX36sZsA==, tableContent=null), ArticleFig(id=1210148035888287992, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 6, caption= Predicted protein-protein interaction networks of CsbZIP transcription factors (TFs) with other proteins in <i>Cannabis sativa</i> using STRING tool. The red circles represent CsbZIP TFs, and the cyan circle represent proteins that interact with CsbZIP TFs , figureFileSmall=ZFTC95fvvhmij2wnTXVr9A==, figureFileBig=efkoN6f45F0RG/xX36sZsA==, tableContent=null), ArticleFig(id=1210148036005728509, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=Jknb3x/n/qdK1n02k+NK9A==, figureFileBig=aeYQRzBArB9Ylrd09fI9dg==, tableContent=null), ArticleFig(id=1210148036093808898, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 7, caption= (A) Expression profiles of <i>CsbZIP</i> genes in different tissues including root, stem, leaves, female flower, male flower and seed. (B) Expression profiles of <i>CsbZIP</i> genes in different stages, S1: Phase Ⅰ; S2: Phase Ⅱ; S3: Phase Ⅲ; S4: Phase Ⅳ; S5: Phase Ⅴ. (C) The expression levels of <i>CsbZIP</i> genes were verified by qRT-PCR , figureFileSmall=Jknb3x/n/qdK1n02k+NK9A==, figureFileBig=aeYQRzBArB9Ylrd09fI9dg==, tableContent=null), ArticleFig(id=1210148036202860809, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=3pRLjt0+EUBUySxiZw3cXg==, figureFileBig=P8PZ3wpbsTub0RTiuHveNw==, tableContent=null), ArticleFig(id=1210148036337078541, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 8, caption= (A) The lipid biosynthesis pathway in <i>Cannabis sativa</i>. Enzymes in this pathway are marked in red words. PDH: Pyruvate dehydrogenase; ACC(BC): Biotin carboxylase subunit of heteromeric acetyl-CoA carboxylase (ACCase); ACC (BCCP): Biotin carboxyl carrier protein of heteromeric ACCase; KAS: Ketoacyl-ACP synthase; KAR: 3-Ketobutyryl-ACP reductase; HAD: 3-Hydroxybutyril-ACP dehydratase; ENR: Enoyl-ACP reductase; SAD: Stearoyl-ACP desaturase; FATA: Acyl-ACP thioesterase A; FATB: Acyl-ACP thioesterase B; LACS: Long-chain acyl-CoA sythetase; GPAT; Glycerol-3-phosphate acyltransferase; LPAT: Lysophosphatidic acid acyltransferase; PAP: Phosphatidic acid phosphatase; DGAT: Diacylglycerol acyhransferase; PDAT: Phospholipid: diacylglycerol acyltransferase; CPT: Diacylglycerol cholinephosphotransferase; FAD2: v-6 desaturase; FAD3: v-3 desaturase; TAG: Triacylglycerol. (B) The prediction of upstream <i>cis</i>-elements of lipid synthesis genes , figureFileSmall=3pRLjt0+EUBUySxiZw3cXg==, figureFileBig=P8PZ3wpbsTub0RTiuHveNw==, tableContent=null), ArticleFig(id=1210148036441936147, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=GOOwMKgziCEPU+lErGO/ew==, figureFileBig=idlGDM1pj3qVo9sWZkuTpg==, tableContent=null), ArticleFig(id=1210148036563570970, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 9, caption= (A) Expression profiles of lipid synthesis genes in different tissues including root, stem, leaves, female flower, male flower and seed. (B) Expression profiles of lipid synthesis genes in different stages, S1: Phase Ⅰ; S2: Phase Ⅱ; S3: Phase Ⅲ; S4: Phase Ⅳ; S5: Phase Ⅴ. (C) The expression levels of lipid synthesis genes were verified by qRT-PCR , figureFileSmall=GOOwMKgziCEPU+lErGO/ew==, figureFileBig=idlGDM1pj3qVo9sWZkuTpg==, tableContent=null), ArticleFig(id=1210148036639068442, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=KyTNX4u4N4cx+XLQtv/p2Q==, figureFileBig=Lpa4wSKtLRH62i0JVo11ww==, tableContent=null), ArticleFig(id=1210148036739731743, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Figure 10, caption= Correlation analysis of <i>CsbZIP</i> genes with lipid synthesis genes. The different colors represent the correlation coefficient , figureFileSmall=KyTNX4u4N4cx+XLQtv/p2Q==, figureFileBig=Lpa4wSKtLRH62i0JVo11ww==, tableContent=null), ArticleFig(id=1210148036840395046, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
GeneForward primer sequence (5′-3′)Reverse primer sequence (5′-3′)
CsbZIP12GTTGGCTGATTTGGCACAGCTTCCCTTTGCTACTCCTAA
CsbZIP13GAGAAACGGGGCTTACACGGGAACAGCCAACCCCATAG
CsbZIP28CTCCCTGATTCTGCTGCCATGGGTCCTTCTTGCTCCG
CsbZIP41CATTTCTGCTGCTGCGGTTCAACATTGTCCAACGCC
CsbZIP42TCAAGTCACTGGAGAGGGCTCTAAATCGCTCAAGTATGCC
CsbZIP43GAGTCCTGCGGTCCAATCCGAGTCTCCACCACCGAA
CsbZIP44GTTTGGGTTTCGGTGGTGCCATCAACGCCAAGACCA
CsHAD-1CTCACTCAACCGACCCACAAACAGAAACGGAAACCGATGG
CsENR-1AGTGGACAGTTCAGGAAGTTGCGTGTTGACTCTAACTCGGTG
CsLACS-4TTTGGTGGTGCTCGTATTGAAGAGAGCGAAGAAGCCG
CsGPAT-3AAGAAAGGCGAATACACGAACACTGACACTCCAACCCCG
CsDGAT-1TCGTCATCATTCCCATCGGCCAGTAAGGTCAGCAAGT
CsPDAT-3TGCTCGGTCTTCAAACGCCAAACCTCACCGCTACACG
CsPDAT-4CCAAAGTTGATGGCACGATAAACCGAGTCTTCCCCC
CsActinTGATGAGTCAGGTCCATCCAGCCTCTCTCAAAAGCAGCAG
), ArticleFig(id=1210148036957835562, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Table 1, caption=

Details of primers for qRT-PCR in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
GeneForward primer sequence (5′-3′)Reverse primer sequence (5′-3′)
CsbZIP12GTTGGCTGATTTGGCACAGCTTCCCTTTGCTACTCCTAA
CsbZIP13GAGAAACGGGGCTTACACGGGAACAGCCAACCCCATAG
CsbZIP28CTCCCTGATTCTGCTGCCATGGGTCCTTCTTGCTCCG
CsbZIP41CATTTCTGCTGCTGCGGTTCAACATTGTCCAACGCC
CsbZIP42TCAAGTCACTGGAGAGGGCTCTAAATCGCTCAAGTATGCC
CsbZIP43GAGTCCTGCGGTCCAATCCGAGTCTCCACCACCGAA
CsbZIP44GTTTGGGTTTCGGTGGTGCCATCAACGCCAAGACCA
CsHAD-1CTCACTCAACCGACCCACAAACAGAAACGGAAACCGATGG
CsENR-1AGTGGACAGTTCAGGAAGTTGCGTGTTGACTCTAACTCGGTG
CsLACS-4TTTGGTGGTGCTCGTATTGAAGAGAGCGAAGAAGCCG
CsGPAT-3AAGAAAGGCGAATACACGAACACTGACACTCCAACCCCG
CsDGAT-1TCGTCATCATTCCCATCGGCCAGTAAGGTCAGCAAGT
CsPDAT-3TGCTCGGTCTTCAAACGCCAAACCTCACCGCTACACG
CsPDAT-4CCAAAGTTGATGGCACGATAAACCGAGTCTTCCCCC
CsActinTGATGAGTCAGGTCCATCCAGCCTCTCTCAAAAGCAGCAG
), ArticleFig(id=1210148037066887468, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
Gene nameGene IDCHrChromosome locationGene length/bpORF length/bpDeduced proteinSubcellular location
Size(aa)MW/kDapIGRAVY
CsbZIP1XP_030490468.11131184-1335292 3451 10036740.886.07-0.95Nucleus
CsbZIP2XP_030490768.1145266477-452715105 03399133237.178.61-0.55Nucleus
CsbZIP3XP_030489233.1179796624-797997333 1091 25142045.658.38-0.85Nucleus
CsbZIP4XP_030506327.12889819-8921152 29692330835.816.81-1.00Nucleus
CsbZIP5XP_030503171.12932250-9384886 2381 28643148.607.81-0.74Nucleus
CsbZIP6XP_030503170.12932250-9392186 9681 60553860.216.72-0.78Nucleus
CsbZIP7XP_030503792.1214777800-147797391 93992730934.196.72-0.68Nucleus
CsbZIP8XP_030505964.1287269479-872719122 4331 20840343.536.07-0.81Nucleus
CsbZIP9XP_030495829.13482152-48289574374324727.705.65-0.79Nucleus
CsbZIP10XP_030493871.134062813-40667443 9311 22141044.476.44-0.83Nucleus
CsbZIP11XP_030495583.1322692505-2269323673173124326.988.69-0.77Nucleus
CsbZIP12XP_030494140.1347006072-470097773 7051 56552357.758.35-0.79Nucleus
CsbZIP13XP_030492683.1380289965-802922882 3231 47949453.506.82-0.92Nucleus
CsbZIP14XP_030498547.1466699237-667022863 0491 07836140.836.48-0.46Nucleus
CsbZIP15XP_030499953.1479302204-793033891 18587629232.119.84-0.86Nucleus
CsbZIP16XP_030498081.1480330869-803345023 63365821925.168.58-0.86Nucleus
CsbZIP17XP_030499008.1483685986-836884832 4971 07536137.805.85-0.86Nucleus
CsbZIP18XP_030498421.1484898096-8489863553953917920.516.29-0.81Nucleus
CsbZIP19XP_030498505.1491804778-918080683 2901 36545649.056.25-0.73Nucleus
CsbZIP20XP_030501220.1533851498-338577366 2381 23141543.966.02-0.88Nucleus
CsbZIP21XP_030501737.1566297971-663023074 33699333136.759.13-0.79Nucleus
CsbZIP22XP_030501753.1566567617-665730525 43597032534.296.99-0.87Nucleus
CsbZIP23XP_030500765.1584545743-845476291 88678626328.815.17-0.94Nucleus
CsbZIP24XP_030510819.1631989647-319908111 16487029032.794.62-0.65Nucleus
CsbZIP25XP_030510247.1672721569-727242622 6931 71257162.246.16-0.91Nucleus
CsbZIP26XP_030510623.1674719303-7471981551251217018.896.51-0.62Nucleus
CsbZIP27XP_030479688.171599399-16014492 05092931034.125.33-0.76Nucleus
CsbZIP28XP_030481936.1826913865-269203306 4651 60053659.977.15-0.71Nucleus
CsbZIP29XP_030482272.1831132156-311389246 7681 39646851.337.81-0.55Nucleus
CsbZIP30XP_030482275.1831134053-311389244 87199133237.058.85-0.63Nucleus
CsbZIP31XP_030481818.1835602476-356061073 6311 46249054.546.1-0.50Nucleus
CsbZIP32XP_030481671.1838542363-3854320283983927932.275.66-1.12Nucleus
CsbZIP33XP_030482255.1851565650-515667931 14382827630.215.82-0.72Nucleus
CsbZIP34XP_030482254.1851565650-515681272 47799533236.666.01-0.82Nucleus
CsbZIP35XP_030482052.1855335000-5533567767767722526.035.65-0.86Nucleus
CsbZIP36XP_030482193.1856575957-565781942 2372 23774580.396.51-0.55Nucleus
CsbZIP37XP_030508159.1950617099-506202623 1631 31343847.836.09-0.86Nucleus
CsbZIP38XP_030486255.1X3101301-31040002 6991 43347851.189.47-0.63Nucleus
CsbZIP39XP_030486266.1X3263820-32665592 7391 43948051.309.47-0.62Nucleus
CsbZIP40XP_030489067.1X9161244-916167543143114316.039.09-0.60Nucleus
CsbZIP41XP_030493109.1X28546514-285465942 51893831334.128.54-0.55Chloroplast
CsbZIP42XP_030495242.1X43111516-431169405 42450016718.309.33-1.12Nucleus
CsbZIP43XP_030497414.1X59123877-591258862 0091 09736640.038.94-0.84Nucleus
CsbZIP44XP_030507823.1X59583168-595851992 03174725028.2210.26-0.91Nucleus
CsbZIP45XP_030499089.1X75289063-752916902 6271 28042745.879.63-0.61Nucleus
CsbZIP46XP_030507426.1X82004861-8200554468346815617.819.37-0.95Nucleus
CsbZIP47XP_030508845.1X82637160-8263800184159119722.279.76-0.82Nucleus
CsbZIP48XP_030508849.1X82637160-8263791975952217419.629.12-0.77Nucleus
CsbZIP49XP_030477746.1X87682842-8768324340140113315.417.76-0.75Nucleus
CsbZIP50XP_030484774.1X102894348-10289487853053017620.266.19-1.01Nucleus
CsbZIP51XP_030485273.1X103452793-1034551822 3891 65255159.856.26-0.83Nucleus
CsbZIP52XP_030485546.1X104179989-1041822522 2631 05035239.775.38-0.61Nucleus
CsbZIP53XP_030485505.1X104179989-1041822922 3031 10437042.296.13-0.59Nucleus
CsbZIP54XP_030485530.1X104180194-1041822922 0981 09936842.106.13-0.59Nucleus
CsbZIP55XP_030485618.1X104347422-1043517484 32698132836.255.95-0.75Nucleus
), ArticleFig(id=1210148037201105203, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1210148022827225533, language=CN, label=Table 2, caption=

Basic information of CsbZIP genes identified in Cannabis sativa

, figureFileSmall=null, figureFileBig=null, tableContent=
Gene nameGene IDCHrChromosome locationGene length/bpORF length/bpDeduced proteinSubcellular location
Size(aa)MW/kDapIGRAVY
CsbZIP1XP_030490468.11131184-1335292 3451 10036740.886.07-0.95Nucleus
CsbZIP2XP_030490768.1145266477-452715105 03399133237.178.61-0.55Nucleus
CsbZIP3XP_030489233.1179796624-797997333 1091 25142045.658.38-0.85Nucleus
CsbZIP4XP_030506327.12889819-8921152 29692330835.816.81-1.00Nucleus
CsbZIP5XP_030503171.12932250-9384886 2381 28643148.607.81-0.74Nucleus
CsbZIP6XP_030503170.12932250-9392186 9681 60553860.216.72-0.78Nucleus
CsbZIP7XP_030503792.1214777800-147797391 93992730934.196.72-0.68Nucleus
CsbZIP8XP_030505964.1287269479-872719122 4331 20840343.536.07-0.81Nucleus
CsbZIP9XP_030495829.13482152-48289574374324727.705.65-0.79Nucleus
CsbZIP10XP_030493871.134062813-40667443 9311 22141044.476.44-0.83Nucleus
CsbZIP11XP_030495583.1322692505-2269323673173124326.988.69-0.77Nucleus
CsbZIP12XP_030494140.1347006072-470097773 7051 56552357.758.35-0.79Nucleus
CsbZIP13XP_030492683.1380289965-802922882 3231 47949453.506.82-0.92Nucleus
CsbZIP14XP_030498547.1466699237-667022863 0491 07836140.836.48-0.46Nucleus
CsbZIP15XP_030499953.1479302204-793033891 18587629232.119.84-0.86Nucleus
CsbZIP16XP_030498081.1480330869-803345023 63365821925.168.58-0.86Nucleus
CsbZIP17XP_030499008.1483685986-836884832 4971 07536137.805.85-0.86Nucleus
CsbZIP18XP_030498421.1484898096-8489863553953917920.516.29-0.81Nucleus
CsbZIP19XP_030498505.1491804778-918080683 2901 36545649.056.25-0.73Nucleus
CsbZIP20XP_030501220.1533851498-338577366 2381 23141543.966.02-0.88Nucleus
CsbZIP21XP_030501737.1566297971-663023074 33699333136.759.13-0.79Nucleus
CsbZIP22XP_030501753.1566567617-665730525 43597032534.296.99-0.87Nucleus
CsbZIP23XP_030500765.1584545743-845476291 88678626328.815.17-0.94Nucleus
CsbZIP24XP_030510819.1631989647-319908111 16487029032.794.62-0.65Nucleus
CsbZIP25XP_030510247.1672721569-727242622 6931 71257162.246.16-0.91Nucleus
CsbZIP26XP_030510623.1674719303-7471981551251217018.896.51-0.62Nucleus
CsbZIP27XP_030479688.171599399-16014492 05092931034.125.33-0.76Nucleus
CsbZIP28XP_030481936.1826913865-269203306 4651 60053659.977.15-0.71Nucleus
CsbZIP29XP_030482272.1831132156-311389246 7681 39646851.337.81-0.55Nucleus
CsbZIP30XP_030482275.1831134053-311389244 87199133237.058.85-0.63Nucleus
CsbZIP31XP_030481818.1835602476-356061073 6311 46249054.546.1-0.50Nucleus
CsbZIP32XP_030481671.1838542363-3854320283983927932.275.66-1.12Nucleus
CsbZIP33XP_030482255.1851565650-515667931 14382827630.215.82-0.72Nucleus
CsbZIP34XP_030482254.1851565650-515681272 47799533236.666.01-0.82Nucleus
CsbZIP35XP_030482052.1855335000-5533567767767722526.035.65-0.86Nucleus
CsbZIP36XP_030482193.1856575957-565781942 2372 23774580.396.51-0.55Nucleus
CsbZIP37XP_030508159.1950617099-506202623 1631 31343847.836.09-0.86Nucleus
CsbZIP38XP_030486255.1X3101301-31040002 6991 43347851.189.47-0.63Nucleus
CsbZIP39XP_030486266.1X3263820-32665592 7391 43948051.309.47-0.62Nucleus
CsbZIP40XP_030489067.1X9161244-916167543143114316.039.09-0.60Nucleus
CsbZIP41XP_030493109.1X28546514-285465942 51893831334.128.54-0.55Chloroplast
CsbZIP42XP_030495242.1X43111516-431169405 42450016718.309.33-1.12Nucleus
CsbZIP43XP_030497414.1X59123877-591258862 0091 09736640.038.94-0.84Nucleus
CsbZIP44XP_030507823.1X59583168-595851992 03174725028.2210.26-0.91Nucleus
CsbZIP45XP_030499089.1X75289063-752916902 6271 28042745.879.63-0.61Nucleus
CsbZIP46XP_030507426.1X82004861-8200554468346815617.819.37-0.95Nucleus
CsbZIP47XP_030508845.1X82637160-8263800184159119722.279.76-0.82Nucleus
CsbZIP48XP_030508849.1X82637160-8263791975952217419.629.12-0.77Nucleus
CsbZIP49XP_030477746.1X87682842-8768324340140113315.417.76-0.75Nucleus
CsbZIP50XP_030484774.1X102894348-10289487853053017620.266.19-1.01Nucleus
CsbZIP51XP_030485273.1X103452793-1034551822 3891 65255159.856.26-0.83Nucleus
CsbZIP52XP_030485546.1X104179989-1041822522 2631 05035239.775.38-0.61Nucleus
CsbZIP53XP_030485505.1X104179989-1041822922 3031 10437042.296.13-0.59Nucleus
CsbZIP54XP_030485530.1X104180194-1041822922 0981 09936842.106.13-0.59Nucleus
CsbZIP55XP_030485618.1X104347422-1043517484 32698132836.255.95-0.75Nucleus
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火麻仁基原植物bZIP基因家族鉴定及其调控油脂代谢的功能初探
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怀浩 1, 2 , 宁康 2 , 侯聪 2 , 杨树明 3 , 汪鋆植 1 , 陈士林 2 , 董林林 2, *
药学学报 | 研究论文 2022,57(8): 2528-2542
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药学学报 | 研究论文 2022, 57(8): 2528-2542
火麻仁基原植物bZIP基因家族鉴定及其调控油脂代谢的功能初探
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怀浩1, 2, 宁康2, 侯聪2, 杨树明3, 汪鋆植1, 陈士林2, 董林林2, *
作者信息
  • 1.三峡大学生物与制药学院, 湖北 宜昌 443002
  • 2.中国中医科学院中药研究所, 北京 100700
  • 3.云南大麻产业投资有限公司, 云南 昆明 650217

通讯作者:

*董林林, E-mail:
The identification of bZIP gene family in Cannabis sativa L. and its preliminary research of the function in regulation of lipid metabolism
Hao HUAI1, 2, Kang NING2, Cong HOU2, Shu-ming YANG3, Jun-zhi WANG1, Shi-lin CHEN2, Lin-lin DONG2, *
Affiliations
  • 1. College of Biological & Pharmaceutical Sciences, China Three Gorges University, Yichang 443002, China
  • 2. Institute of Chinese Meteria Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China
  • 3. Yunnan Hemp Industrial Investment Co. Ltd., Kunming 650217, China
出版时间: 2022-08-12 doi: 10.16438/j.0513-4870.2022-0440
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摘要
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bZIP (basic leucine zipper) 基因家族是真核生物中最大的转录因子家族之一, 其成员在逆境响应、次级代谢、植物生长、种子发育等方面发挥着重要作用。为探究火麻仁基原植物大麻(Cannabis sativa L.) bZIP (CsbZIP) 基因的生物学功能, 本研究基于大麻全基因组和转录组数据, 利用生物信息学方法对CsbZIP基因家族进行系统性研究。结果表明, 在大麻中鉴定到55个CsbZIP基因家族成员(CsbZIP1~CsbZIP55), 分布在10条染色体上, 属于12个亚家族, 同一亚家族成员之间的基因结构和蛋白基序分布相似。片段重复是CsbZIP基因家族扩张的主要因素。顺式作用元件分析表明73个油脂合成基因的启动子区含有G-box或A-box元件, qRT-PCR实验表明7个CsbZIP基因和7个油脂合成基因在火麻仁中的相对表达量较高。相关性分析表明7个CsbZIP基因和7个油脂合成基因之间存在显著的正相关关系。本研究揭示了CsbZIP基因的结构特征、进化方式和表达模式, 为进一步研究CsbZIP基因对火麻仁油脂代谢的调控提供了重要线索。

火麻仁  /  药用大麻  /  bZIP基因家族  /  油脂代谢  /  表达模式

The bZIP (basic leucine zipper) gene family is one of the largest transcription factor families in eukaryotes, and its members play important roles in stress response, secondary metabolism, plant growth, seed development and other aspects. To investigate the biological functions of the bZIP (CsbZIP) gene in Cannabis sativa L., we systematically investigated the CsbZIP gene family using bioinformatics methods based on the whole-genome and transcriptome data. The results showed that 55 CsbZIP gene family members (CsbZIP1-CsbZIP55) were identified and distributed on 10 chromosomes, belonging to 12 subfamilies. The gene structure and protein motif distribution of the same subfamily members were similar. Segment repeats were the main reasons for the expansion of CsbZIP gene family. Cis-elements analysis showed that the promoter regions of 73 lipid synthesis genes contained G-box or A-box element. qRT-PCR showed that the relative expression levels of 7 CsbZIP genes and 7 lipid synthesis genes were relatively high in hemp seed. 7 CsbZIP genes had a significant positive correlation with 7 lipid synthesis genes. This study revealed the structural features, evolutionary patterns and expression patterns of CsbZIP, providing important clues for further study on the regulation of CsbZIP on oil metabolism of hemp seed.

hemp seed  /  non-psychoactive medicinal cannabis  /  bZIP gene family  /  lipid metabolism  /  expression profile
怀浩, 宁康, 侯聪, 杨树明, 汪鋆植, 陈士林, 董林林. 火麻仁基原植物bZIP基因家族鉴定及其调控油脂代谢的功能初探. 药学学报, 2022 , 57 (8) : 2528 -2542 . DOI: 10.16438/j.0513-4870.2022-0440
Hao HUAI, Kang NING, Cong HOU, Shu-ming YANG, Jun-zhi WANG, Shi-lin CHEN, Lin-lin DONG. The identification of bZIP gene family in Cannabis sativa L. and its preliminary research of the function in regulation of lipid metabolism[J]. Acta Pharmaceutica Sinica, 2022 , 57 (8) : 2528 -2542 . DOI: 10.16438/j.0513-4870.2022-0440
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亮氨酸拉链(basic leucine zipper, bZIP) 是广泛分布于真核生物中的一类可编码转录因子的超基因家族[1]。植物bZIP转录因子含有两个功能域: 一个基本区域和一个相邻的亮氨酸拉链, 基本区域在真核生物中非常保守, 是DNA结合域, 一般由18个氨基酸残基组成, 具有相同的氨基酸序列模型(N-X7-R/K-X9)[2]。亮氨酸拉链区由重复氨基酸序列L-X6-L-X6-L组成, 该区域变化较大, 亮氨酸位于七肽序列的第7个氨基酸位置, 可以被异亮氨酸、缬氨酸、苯丙氨酸或蛋氨酸取代[3, 4]。植物bZIP转录因子偏好ACGT核心序列, 如A-box (TACGTA)、C-box (GACGTC)、G-box (CACGTG)[5]。bZIP蛋白一般通过亮氨酸拉链形成二聚体来发挥作用, 依赖基本区域与DNA结合, 从而实现对基因的灵活调控[2]。
bZIP转录因子广泛参与植物的生长发育和胁迫响应等多种生命活动[6]。例如, 种子萌发[7]、花器官的发育[8]、胁迫应答[9]、次生代谢[10]。在拟南芥中, AtbZIP29可以调控根尖分生组织细胞中细胞壁形成有关基因的表达, 从而影响根的生长发育[11]。在番茄中过表达SlAREB基因可以提高植株对水分和盐胁迫的耐受性[12]。bZIP转录因子可调控植物的次生代谢, 研究表明过表达SmbZIP1基因可抑制丹参酮的积累, 而利用基因编辑技术敲除SmbZIP1基因可显著提高丹参酮含量[13]。bZIP转录因子在植物生长发育的调控、胁迫应答、次生代谢和信号介导中具有重要作用。
大麻(Cannabis sativa L.) 属于大麻科(Cannabinaceae) 大麻属(Cannabis), 一年生草本植物, 起源于亚欧大陆, 有着悠久的种植历史, 在世界各地广泛种植[14]。宁康等[15]将四氢大麻酚(THC) 质量分数小于0.3%且大麻二酚(CBD) 含量高(原则上应大于2.0%) 的大麻定义为非精神活性药用大麻。火麻仁, 即大麻的种子, 是一种良好的药食同源材料, 《神农本草经》对火麻仁的描述为“麻子, 味甘, 性平。主补中益气, 肥健不老”, 火麻仁归脾、胃、大肠经, 具有润肠通便、缓解月经紊乱、通淋活血等功效[16, 17], 此外火麻仁还被开发成火麻油、饮料和高蛋白营养品等[18]。火麻仁富含油脂、蛋白质、多种微量元素以及黄酮和酚类物质, 其中油脂含量占27.04%~37.67%, 而油脂中含量最多的是不饱和脂肪酸, 占比高达77.55%~81.21%[17]。油脂是火麻仁中的一类重要的物质, 其中富含的不饱和脂肪酸具有重要的营养价值和药理作用[19]。现代临床研究表明, 火麻仁富含的不饱和脂肪酸具有降血糖血脂、抗炎镇痛、改善肠道微环境、减轻肠道炎症反应等功效[20]。然而, 目前关于火麻仁油脂合成的分子机制尚不清楚, 因此, 探究火麻仁油脂合成调控机制的分子基础, 挖掘油脂合成关键基因和转录调控因子, 对于培育高油脂含量的火麻仁基原植物具有重要意义。
bZIP基因家族的鉴定和系统性研究在许多植物中均有报道, 例如拟南芥[4]、水稻[21]、葡萄[22]、玉米[23]、油菜[24]、高粱[25]和大豆[26]等。bZIP转录因子在调控油脂合成过程中有着重要的作用[2]。在拟南芥中, AtbZIP67转录因子能够结合FAD3基因启动子区的G-box作用元件, 增强FAD3基因的表达, 从而提高了拟南芥种子中ω-3多不饱和脂肪酸的含量[27]。GmbZIP123基因可参与大豆种子脂质积累的调控, 研究发现, 在转基因拟南芥中过表达GmbZIP123可提高拟南芥种子的脂质含量[28]。bZIP基因在大麻中的研究还未曾报道过, 且CsbZIP基因调控火麻仁油脂代谢的相关研究亦未见报道。
鉴于bZIP基因家族在调控油脂代谢中的重要作用, 以及该基因家族在大麻中尚未鉴定且功能缺少系统性研究。因此, 本研究基于大麻全基因组数据, 对大麻bZIP基因家族进行了系统性研究, 包括家族成员鉴定、序列特征分析、系统发育分析、基因结构及保守基序(motif) 分析、共线性关系分析、蛋白互作网络分析及表达模式分析。此外, 基于转录组数据, 构建了火麻仁油脂生物合成通路, 分析了油脂合成基因的表达水平, 并对CsbZIP基因和油脂合成基因进行了相关性分析, 为进一步研究CsbZIP基因在油脂代谢中的作用提供基础。
材料与方法
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材料  本研究所用的大麻品种为非精神活性药用大麻, 即THC质量分数小于0.3%且CBD含量高的大麻品种[15]。大麻全基因组数据和全基因组注释文件均来自NCBI数据库(https://www.ncbi.nlm.nih.gov/), 大麻AA126品种植株的根、茎、叶、雌花、雄花和种子及5个不同的发育时期(5个时期依据种子的发育状态来定义, S1: 第一阶段, 顶端分生组织, 雌花未出现; S2: 第二阶段, 此时雌花已出现, 柱头呈现白色; S3: 第三阶段, 此时授粉完成, 柱头呈现橙色; S4: 第四阶段, 此时种子呈现绿色尚未成熟; S5: 第五阶段, 此时种子成熟且呈现出棕褐色) 的RNA-seq数据由本课题组提供[16]。拟南芥、葡萄、水稻及玉米的全基因组、全基因组注释文件及蛋白质文件均来自Ensembl Plants数据库(https://plants.ensembl.org/index.html)。
CsbZIP基因的鉴定及蛋白序列特征分析  使用TBtools软件来提取拟南芥bZIP蛋白序列用作查询, 对大麻蛋白质数据库进行BLASTP搜索(value为1×10-5)。从PFAM数据库(http://pfam.xfam.org/) 中下载bZIP蛋白的Hidden Markov模型(PF00170), 基于大麻蛋白质数据库, 通过HMMER 3.0软件搜索具有该结构域的蛋白(value为1×10-5)。合并去重后将剩余序列提交到NCBI-CDD (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi) 和PFAM (http://pfam.xfam.org/) 数据库中来验证bZIP蛋白的保守域。依据它们的染色体位置命名, 使用ExPASy (https://web.expasy.org/protparam/) 分析蛋白质的理化性质, 利用CELLO v2.5 (http://cello.life.nctu.edu.tw/) 进行亚细胞定位分析。
CsbZIP基因的系统发育分析  采用ClustalW工具对已鉴定到的55条CsbZIP蛋白序列和77条拟南芥bZIP蛋白序列(AtbZIP53由于序列差异太大被排除) 进行多序列比对[4], 然后利用MGEA7.0软件构建系统发育树, 采用NJ邻接法, bootstrap值设置为1 000。CsbZIP蛋白的分类方法参考拟南芥之前的研究[4]。
CsbZIP基因的结构及保守基序分析  基于大麻全基因组注释信息, 使用Gene Structure Display Server (GSDS2.0) (http://gsds.gao-lab.org/index.php) 来展示基因的结构。使用MEME在线工具(http://meme-suite.org/) 分析CsbZIP蛋白的保守基序。最大motif数设置为10。通过TBtools软件可视化, 利用NCBI-CDD数据库分析motif的注释信息。
CsbZIP基因的染色体定位、基因复制事件和共线性分析  根据CsbZIP基因在大麻基因组中的位置信息, 用MapChart软件绘制CsbZIP基因在染色体上的位置。利用多重共线性扫描工具(multiple collinearity scan toolkit, McScanx) 分析基因复制事件, 使用TBtools软件自带的Dual Systeny Plotter工具分析大麻和其他4个物种(拟南芥、葡萄、水稻、玉米) 的bZIP基因之间的共线关系。
CsbZIP基因的互作网络分析   基于拟南芥和大麻之间的bZIP基因的同源关系, 使用STRING数据库(https://string-db.org/) 研究CsbZIP基因的互作网络。利用Cytoscape软件来展示预测的互作网络。
基因的表达分析  利用本课题组前期自测的转录组数据来分析CsbZIP基因和油脂合成基因的表达模式, 基于FPKM值, 利用在线云平台工具(https://www.omicstudio.cn/index) 绘制热图, 进行可视化分析。
油脂合成基因的启动子区顺式作用元件分析  利用TBtools工具提取86个油脂合成基因的启动子区序列(上游2 kb), 然后提交到PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) 数据库来预测顺式作用元件。利用TBtools工具进行可视化。
植物RNA的提取和qRT-PCR  采用快速RNA提取试剂盒(北京华越洋生物科技有限公司), 按照生产厂家的说明书来提取总RNA。使用KR118反转录试剂盒(天根生化科技(北京) 有限公司) 通过一步法合成cDNA。采用Primer 5.0软件设计引物(表 1), 以Actin基因作为内参基因, 引物合成由擎科生物科技公司完成。使用StarLighter SYBR Green qPCR Mix试剂盒(北京启衡星生物科技有限公司) 进行qRT-PCR实验。反应程序为: 95 ℃酶激活5 min, 95 ℃变性30 s, 60 ℃退火30 s, 72 ℃延伸1 s, 循环次数为40。基因的相对表达量采用2-ΔΔCt方法计算。
相关性分析  基于CsbZIP基因和油脂合成基因之间的表达水平, 利用R语言进行Spearman相关性分析并可视化。
结果与分析
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1 CsbZIP基因的鉴定及理化性质分析
通过HMMER和BLASTP比对方法分别鉴定到了92个和129个CsbZIP基因, 合并去除重复后使用NCBI-CDD和Pfam数据库来验证保守域, 最终鉴定到55个CsbZIP基因, 依据它们在染色体上的位置进行命名(CsbZIP1~CsbZIP55)。蛋白序列特征分析表明, 55个CsbZIP基因的编码蛋白的长度范围在133~745个氨基酸之间, 平均长度为348个氨基酸。蛋白质分子质量介于15.41~80.39 kDa, 平均蛋白质分子质量为38.38 kDa; 理论等电点介于4.62~10.26, 平均等电点为7.25, GRAVY均为负值, 表明这些CsbZIP蛋白均为亲水性蛋白。亚细胞定位预测结果表明只有CsbZIP41蛋白定位于叶绿体中, 其他的CsbZIP蛋白均定位于细胞核内(表 2)。
2 CsbZIP基因的系统发育分析
利用CsbZIP基因的氨基酸序列和拟南芥bZIP基因进行多序列比对, 分析CsbZIP基因家族的进化关系(图 1)。系统发育树表明CsbZIP基因可分成12个亚家族, 这12个亚家族分别是A、B、C、D、E、F、G、H、I、J、K和S, 分别含有12、1、2、11、3、1、6、1、7、1、1和9个CsbZIP基因, 其中最大的3个亚家族分别是A、D和S。
3 CsbZIP基因结构和保守基序分析
通过分析CsbZIP基因的内含子和外显子分布, 进一步研究其结构特征。系统发育分析表明同一亚家族内的基因通常具有相似的内含子和外显子结构(图 2)。这些CsbZIP基因的外显子数量范围在1~12之间, 有10个CsbZIP基因(18.18%) 只含有一个外显子, 其中绝大多数是S亚家族成员。D亚家族中的成员含有外显子的数量范围在8~12之间; 亚家族G含有6~12个外显子; 亚家族A含有3~6个外显子。这些结构特征可能与它们在基因组中的功能有关。
在55个CsbZIP蛋白中鉴定到了10个保守的motif结构, 同一亚家族蛋白成员之间的motif分布相似(图 2)。Motif1普遍存在于所有CsbZIP蛋白中, 代表着高度保守的亮氨酸拉链结构域(leucine zipper domain)。Motif2只存在于亚家族D和亚家族K中; motif3、motif4、motif6和motif10只存在于亚家族D中。亚家族E和I的每个成员均含有motif5, CsbZIP23蛋白(亚家族G)、CsbZIP41蛋白(亚家族A) 和CsbZIP19蛋白(亚家族C) 也都含有motif5; 除了CsbZIP17蛋白(亚家族G), CsbZIP33蛋白(亚家族E) 和CsbZIP19蛋白(亚家族C) 不含有motif7, 其他的所有CsbZIP蛋白均含有motif7; motif8只存在于亚家族D的这3个成员中(CsbZIP52、CsbZIP53和CsbZIP54); motif9只存在于亚家族A的这8个成员中(CsbZIP41、CsbZIP7、CsbZIP21、CsbZIP4、CsbZIP13、CsbZIP45、CsbZIP38和CsbZIP39)。系统发育分析结果与内含子/外显子分布和motif分布一致, 表明同一亚家族CsbZIP基因的结构差异较低, 进化关系密切, 保守程度较高。
4 CsbZIP基因的染色体定位、基因复制事件和共线性分析
55个CsbZIP基因不均匀地分布在大麻的10条染色体上(图 3)。其中X染色体上的基因数量最多, 有18个, 9号染色体上最少, 只有1个。染色体的长度和染色体上基因的数量之间不存在正相关关系。
在55个CsbZIP基因中鉴定到6对片段重复事件, 涉及9个CsbZIP基因, CsbZIP38 (亚家族A) 和rna-XM 030630405.1 (由于基因组数据不完整, 所以该基因在基因组注释信息中没有被成功注释, 因此这一对片段重复基因在图 4中没有展示出来); CsbZIP50 (亚家族S) 和CsbZIP18 (亚家族S); CsbZIP50 (亚家族S) 和CsbZIP26 (亚家族S); CsbZIP1 (亚家族I) 和CsbZIP8 (亚家族I); CsbZIP18 (亚家族S) 和CsbZIP26 (亚家族S); CsbZIP32 (亚家族S) 和CsbZIP35 (亚家族S)。结果表明, 形成一个基因复制事件的一对基因来自同一亚家族, 其中大部分都是亚家族S中的基因(图 4)。然而, CsbZIP基因家族中不存在串联重复事件。这些结果表明片段重复事件是CsbZIP基因家族扩张的主要驱动因素。
为了探究bZIP基因在不同物种中的进化关系, 对大麻和4种有代表性的植物进行了基因共线性分析(图 5), 包括2种单子叶植物(水稻和玉米) 和2种双子叶植物(拟南芥和葡萄)。大麻和葡萄之间存在36个bZIP基因对, 其次分别是拟南芥(18对)、水稻(10对)、玉米(5对)。结果表明, 与单子叶植物相比, CsbZIP的共线基因对更多的出现在双子叶植物中。此外, CsbZIP1和CsbZIP40在大麻和其他4种植物之间均存在共线对, 表明在双子叶植物和单子叶植物分化之前, 这些同源基因对可能已经存在。然而, 有6个CsbZIP基因(CsbZIP14、CsbZIP18、CsbZIP25、CsbZIP31、CsbZIP37和CsbZIP50) 的共线对只存在于拟南芥和葡萄中, 而在水稻和玉米中不存在。结果表明, 这些特殊的共线基因对可能是在双子叶植物和单子叶植物分化后形成的。
5 CsbZIP基因的互作网络分析
为了进一步研究CsbZIP基因的生物学功能, 基于CsbZIP基因与拟南芥之间的同源关系构建了CsbZIP基因的蛋白互作网络(图 6)。发现了26个与拟南芥同源的CsbZIP基因和141个与之相互作用的基因。这些互作基因包括一些重要的转录调控因子, 如bZIP、WRKY和MYB; 一些调控植物生长发育的基因, 如SNRK、ROXY、CRP、IRE和SPA。还有一些参与植物信号转导的基因, 如ABI1、KEG和AFP等。结果表明CsbZIP基因在大麻中的作用非常重要, 广泛参与各种生命活动过程。
6 CsbZIP基因的表达分析
为了研究CsbZIP基因的表达模式, 基于大麻的不同组织和不同生长时期的转录组数据绘制了热图。结果表明, 有些CsbZIP基因的表达呈现出明显的组织特异性, 如CsbZIP4、CsbZIP11和CsbZIP46只在雌花中高表达。CsbZIP12和CsbZIP13只在种子中高表达, CsbZIP24和CsbZIP40只在根中高表达。有些基因在不同的组织器官中均有表达, 如CsbZIP28在雄花和种子中的表达水平均较高, CsbZIP14和CsbZIP52在根和茎中的表达水平较高, CsbZIP45在根、茎、叶和花(雌花和雄花) 中都有较高的表达水平。有些基因在所有的组织器官内不表达或表达水平极低, 如CsbZIP16、CsbZIP27、CsbZIP46、CsbZIP48和CsbZIP49 (图 7A)。
在不同的发育时期中, CsbZIP基因的表达情况也类似。有些基因的表达水平表现出明显的时期特异性, 如CsbZIP13和CsbZIP26只在S4时期有较高的表达水平; CsbZIP15和CsbZIP33只在S1时期高表达。有些基因在不同的时期均有较高的表达水平, 如CsbZIP4在S3和S4时期的表达水平较高; CsbZIP18在S3、S4、S5时期的表达水平较高; CsbZIP24、CsbZIP30、CsbZIP36和CsbZIP41在5个时期都有较高的表达水平。有些基因在所有时期内几乎不表达或表达水平极低, 如CsbZIP5、CsbZIP11和CsbZIP16 (图 7B)。表达模式分析结果表明CsbZIP基因成员在大麻的不同组织器官和不同发育时期中的表达均存在差异性, 说明CsbZIP基因之间已出现功能分化。
依据基因在转录组中的表达水平, 以根为对照组, 以种子为实验组, 从中挑选了7个有代表性的基因(CsbZIP12、CsbZIP13、CsbZIP28、CsbZIP41、CsbZIP42、CsbZIP43和CsbZIP44), 利用qRT-PCR实验研究基因的表达水平。结果表明, 这7个CsbZIP基因在种子中的表达水平较高(图 7C), 表明这些基因可能在种子的生长发育中有着重要的调控作用。此外, qRT-PCR实验结果与转录组数据保持一致, 表明转录组数据是可靠的。
7 油脂合成基因的表达分析
基于已有的研究[29], 构建了火麻仁油脂合成通路(图 8A), 在转录组数据中共鉴定到86个油脂合成基因, 对这些油脂合成基因进行启动子区顺式作用元件分析, 结果表明, 有73个油脂合成基因的启动子区含有G-box或A-box作用元件(图 8B), 因此, 对这73个油脂合成基因的表达水平进行分析。转录组数据表明, 有些油脂合成基因的表达存在组织特异性, 如KASⅡ-1、LACS-7、LACS15、LACS16和LACS17只在雄花中高表达; SAD-8只在雌花中高表达; FAD3-1在根中的表达水平显著高于其他组织器官, FAD3-2在叶中的表达水平显著高于其他组织器官。有些基因在不同的组织器官内均有表达, 如PDH-2、PDH-3、PDH-4、PDH-5和ACC-1; FATA-3在叶、雌花、雄花内高表达, 而在根、茎和种子内几乎不表达。有些基因在所有组织器官内不表达或表达水平极低, 如FATB-2、PDAT-9、FAD2-4、FAD2-9和FAD2-11 (图 9A)。
在不同的发育时期中, 油脂合成基因的表达情况类似。有些基因只在特定的时期表达, 如LACS-13和FAD2-11只在S4时期表达, 而在其他时期不表达或表达水平极低。有些基因在不同的时期均有表达, 如PDH-2、PDH-3、PDH-4和PDH-5在5个发育时期中均有表达。有些基因在所有时期中几乎不表达或表达水平极低, 如FATA-1、FATA-2、FATB-2、LACS-7、PDAT-7、PDAT-9和FAD2-9 (图 9B)。
基于油脂合成基因的表达水平以及启动子区的顺式作用元件预测结果, 筛选了7个油脂合成基因(HAD-1、ENR-1、LACS-4、GPAT-3、DGAT-1、PDAT-3和PDAT-4), 以根为对照组, 种子为实验组, 使用qRT-PCR实验研究基因的表达水平(图 9C)。结果表明, 这7个油脂合成基因在种子中有较高的表达水平, 表明这些油脂合成基因的表达可能会影响火麻仁的生长发育。
8 CsbZIP基因与油脂合成基因之间的相关性分析
基于转录组数据, 对7个CsbZIP基因和7个油脂合成基因进行相关性分析(图 10), 结果显示, CsbZIP12与GPAT-3/PDAT-3之间存在显著正相关关系; CsbZIP13与GPAT-3/PDAT-4之间存在显著正相关关系; CsbZIP28与LACS-4/DGAT-1/PDAT-3之间存在显著正相关关系; CsbZIP41与HAD-1之间存在显著正相关关系; CsbZIP42与GPAT-3之间存在显著正相关关系; CsbZIP43与LACS-4/DGAT-1/PDAT-3/PDAT-4之间存在显著正相关关系; CsbZIP44与HAD-1/ENR-1/LACS-4/DGAT-1/PDAT-4之间存在显著正相关关系。结果表明CsbZIP基因可能对油脂合成基因的表达具有调控作用, 从而影响火麻仁中油脂的积累。
讨论
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本研究在大麻中共鉴定到55个CsbZIP基因, 利用生物信息学方法对55个CsbZIP基因进行了系统性研究, 结果表明55个CsbZIP基因的编码蛋白长度范围介于133~745个氨基酸之间; 蛋白质分子质量介于15.41~80.39 kDa。55个CsbZIP基因可分成12个亚家族, 同一亚家族成员之间的基因结构分布相似。片段重复事件是CsbZIP基因家族扩张的主要驱动因素。表达模式分析结果表明7个CsbZIP基因(CsbZIP12、CsbZIP13、CsbZIP28、CsbZIP41、CsbZIP42、CsbZIP43和CsbZIP44) 和7个油脂合成通路基因(HAD-1、ENR-1、LACS-4、GPAT-3、DGAT-1、PDAT-3和PDAT-4) 在火麻仁中的相对表达水平较高。顺式作用元件分析表明上述7个油脂合成基因的启动子区含有A-box或G-box作用元件。相关性分析表明上述7个CsbZIP基因和7个油脂合成基因之间的表达水平存在显著的正相关关系。结果表明, CsbZIP转录因子可能对火麻仁油脂代谢具有重要的调控作用。
bZIP基因家族是植物中最大的转录因子家族之一, 可参与多种生物学过程, 包括植物生长发育的调控、生物和非生物胁迫响应、次级代谢物质的生物合成[30]。bZIP基因在一些物种中已经被报道过, 如拟南芥[4]、水稻[21]、葡萄[22]、玉米[23]等。相比较于拟南芥、水稻和玉米, 大麻中的bZIP基因的数量较少, 只有55个, 与葡萄中bZIP基因的数量一致, 物种间的共线性关系也表明, CsbZIP基因与葡萄bZIP基因之间的共线对的数量最多, 表明大麻与葡萄之间的亲缘关系更密切。亚细胞定位预测结果显示除了CsbZIP41蛋白定位在叶绿体上, 其他的家族成员都定位在细胞核中, 表明CsbZIP转录因子主要在细胞核内发挥作用, 而CsbZIP41转录因子则可能在叶绿体中发挥特殊的作用, 这与油桐中的报道类似[31]。
系统发育分析结果表明, 55个CsbZIP基因可分成12个亚家族。拟南芥的78个bZIP基因被分成13个亚家族[4], 与拟南芥相比较, 大麻缺少M亚家族。研究表明, 葡萄bZIP基因可分成10个亚家族, 缺少K、M和S亚家族[22]。芝麻bZIP基因可分成9个亚家族, 缺少E、J、K和M亚家族[32]。由此可见, 在植物bZIP基因亚家族中, 存在基因缺失事件, CsbZIP基因的亚家族缺失可能是由于该家族成员在进化过程中被丢失。
基因结构分析表明, CsbZIP基因含有1~12个外显子, 其中18%的基因只含有一个外显子, 它们绝大多数分布在S亚家族中, 研究表明, S亚家族的成员通常与C亚家族的成员互作形成二聚体, 在植物的能量代谢调控过程中发挥着关键的作用[4]。例如, 在拟南芥中, bZIP63转录因子可与S亚家族的其他成员结合形成二聚体结构, 促进支链氨基酸的分解代谢, 提供ATP以维持植物在逆境中的生存[33, 34]。D亚家族的成员含有8~12个外显子, 大多数D亚家族成员可介导水杨酸、茉莉酸等激素信号通路来提高植物在生物胁迫下的耐受性[4]。结果表明, 不同亚家族成员之间的基因结构不同, 可能有着不同的生物学功能。同一亚家族中的内含子/外显子结构和motif的排列分布相似, 并倾向于执行相同的生物学功能。例如, 同属于H亚家族的拟南芥AtHY5蛋白和水稻OsbZIP48蛋白分别在双子叶和单子叶系统的光形态建成中发挥重要作用[35]。值得关注的是, 有些motif只存在于特定的亚家族中, 如Motif2只存在于亚家族D和亚家族K中, 鉴于bZIP转录因子的功能多样性, 有些motif可能具备一些特殊的功能, 需要进一步深入研究。
基因复制事件是遗传系统进化的主要驱动因素之一, 其中串联重复和片段重复是植物基因家族扩张的两个主要因素[36, 37]。本次研究鉴定到6对片段重复基因, 占CsbZIP基因的14.5%。但是, 没有一对CsbZIP基因被鉴定为串联重复, 表明在CsbZIP基因家族的进化和扩张过程中, 片段重复事件起着重要作用, 这与葡萄、芝麻和水稻中的研究一致[21, 22, 32]。物种间共线性分析结果表明, 大麻与双子叶植物之间的共线性基因对的数量显著多于单子叶植物, 表明在物种进化过程中, 亲缘关系相对密切的物种, 有更多的共线基因对, 例如大麻和葡萄。此外, 有6个CsbZIP基因(CsbZIP14、CsbZIP18、CsbZIP25、CsbZIP31、CsbZIP37和CsbZIP50) 的共线对只存在于双子叶中, 而在单子叶中不存在, 说明这些特殊的共线基因对可能出现在双子叶植物和单子叶植物分化之后。
bZIP基因家族参与植物的生长发育过程, 包括花的发育和种子的成熟[3, 8]。为了探究CsbZIP基因的生物学功能, 对CsbZIP基因在大麻的不同组织器官和不同发育阶段中的表达模式进行分析, 研究表明, 虽然大多数CsbZIP基因在所有组织中均有表达, 但仍有一些CsbZIP基因在不同组织中的表达存在显著差异, 这与水稻、玉米和葡萄中的研究一致[21-23]。例如, 在大麻中, CsbZIP4基因只在雌花中特异性表达, CsbZIP13基因只在种子中特异性表达, 表明它们可能在大麻特定的组织器官发育中发挥关键作用。
基于拟南芥同源基因, 构建了CsbZIP转录因子的蛋白互作网络。在CsbZIP基因家族蛋白网络互作分析中, CsbZIP12基因与AT1G19490.1基因互为同源基因, 研究表明AT1G19490.1基因的编码蛋白是AtbZIP62转录因子, 该转录因子在拟南芥中可与其他bZIP转录因子互作, 调控拟南芥对干旱胁迫的响应[38]。基于同源基因的功能相似性, 推测CsbZIP12基因可能在大麻参与逆境胁迫响应中发挥作用。CsbZIP13基因与ABI5基因互为同源基因, 在拟南芥中, ABI5基因是种子发育、萌发和幼苗生长所必需的[39]。蛋白互作网络图显示ABI3蛋白、SNRK2.2蛋白、AFP2蛋白等多种蛋白都能与ABI5蛋白发生相互作用。转录组表达谱聚类分析表明, CsbZIP13基因不仅在大麻的种子中高表达, 并且在火麻仁成熟发育期高表达。因此, 基于CsbZIP13基因与ABI5基因之间的同源关系, 推测CsbZIP13基因在大麻中可能与多种蛋白相互作用共同调控火麻仁的生长发育。
研究表明, 在植物中, HAD、ENR、LACS、GPAT、DGAT和PDAT基因的表达会影响油脂的积累[40, 41]。在本次研究中, 转录组数据及qRT-PCR实验结果均表明HAD-1、ENR-1、LACS-4、GPAT-3、DGAT-1、PDAT-3和PDAT-4在火麻仁中的表达水平较高。顺式作用元件分析结果表明, 这7个油脂合成基因的启动子区存在A-box或G-box作用元件, bZIP转录因子可以通过A-box或G-box作用元件与基因结合, 从而调控基因的表达[42]。相关性分析结果表明, 7个CsbZIP基因(CsbZIP12、CsbZIP13、CsbZIP28、CsbZIP41、CsbZIP42、CsbZIP43和CsbZIP44) 的表达水平与7个油脂合成基因(HAD-1、ENR-1、LACS-4、GPAT-3、DGAT-1、PDAT-3和PDAT-4) 的表达水平之间存在显著的正相关。这些结果表明, 在火麻仁中, CsbZIP转录因子可能通过调控油脂合成代谢基因的表达, 从而影响火麻仁中油脂含量的积累。
本研究利用生物信息学方法对CsbZIP基因家族进行了系统性研究, 解析了CsbZIP基因的结构特征、进化方式和表达模式。此外, 基于转录组数据, 构建了火麻仁油脂代谢通路, 预测了火麻仁油脂生物合成基因启动子区的顺式作用元件, 并对油脂合成基因和CsbZIP基因的表达水平进行了相关性分析, 初步筛选出了与火麻仁油脂代谢相关的CsbZIP转录因子。为后续深入研究CsbZIP转录因子在火麻仁油脂代谢调控机制中的作用提供了重要的参考。
作者贡献: 怀浩负责文章撰写及数据分析; 董林林、宁康负责实验设计及论文修改; 侯聪、杨树明负责数据分析和实验材料的收集; 汪鋆植、陈士林指导文章撰写并提出修改意见; 董林林负责论文设计及项目开展。
利益冲突: 所有作者均声明不存在利益冲突。
基金
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  • 海南省院士创新平台科研项目(SQ2021PTZ0052)
  • 国家重点研发计划资助: 中药多组学方法创新及新品种选育研究(2019YFC1711100)
  • 高品质工业大麻品种培育及开发研究(H2021038)
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2022年第57卷第8期
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doi: 10.16438/j.0513-4870.2022-0440
  • 接收时间：2022-04-13
  • 首发时间：2025-12-23
  • 出版时间：2022-08-12
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  • 收稿日期：2022-04-13
  • 修回日期：2022-05-05
基金
海南省院士创新平台科研项目(SQ2021PTZ0052)
国家重点研发计划资助: 中药多组学方法创新及新品种选育研究(2019YFC1711100)
高品质工业大麻品种培育及开发研究(H2021038)
作者信息
    1.三峡大学生物与制药学院, 湖北 宜昌 443002
    2.中国中医科学院中药研究所, 北京 100700
    3.云南大麻产业投资有限公司, 云南 昆明 650217

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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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