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Article(id=1276597973786169707, tenantId=1146029695717560320, journalId=1235980609244409860, issueId=1276597973173801322, articleNumber=null, orderNo=null, doi=10.3969/j.issn.1000-2561.2024.07.005, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1687795200000, receivedDateStr=2023-06-27, revisedDate=1689609600000, revisedDateStr=2023-07-18, acceptedDate=null, acceptedDateStr=null, onlineDate=1782294274993, onlineDateStr=2026-06-24, pubDate=1721836800000, pubDateStr=2024-07-25, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1782294274993, onlineIssueDateStr=2026-06-24, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1782294274993, creator=13701087609, updateTime=1782294274993, updator=13701087609, issue=Issue{id=1276597973173801322, tenantId=1146029695717560320, journalId=1235980609244409860, year='2024', volume='45', issue='7', pageStart='1303', pageEnd='1520', issueExtLink='null', onlineDate='null', pubDate='1721836800000', pubDateStr='2024-07-25', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1782294274847, creator='13701087609', updateTime=1782294274847, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext=null, issueFiles=null, downloadFileDto=null}, startPage=1340, endPage=1347, ext={EN=ArticleExt(id=1276597974088159597, articleId=1276597973786169707, tenantId=1146029695717560320, journalId=1235980609244409860, language=EN, title=Cloning, Subcellular Localization, and Expression Analysis of CePIP2;1, an Aquaporin Gene from Tigernut (Cyperus esculentus L.), columnId=1236256430337085821, journalTitle=Chinese Journal of Tropical Crops, columnName=Omics & Biotechnology, runingTitle=null, highlight=null, articleAbstract=

Tigernut (Cyperus esculentus L.) is an herbaceous oil crop uniquely accumulating a high level of oil in the underground tubers. Water, which accounts for approximately 85% of immature tubers, is essential for tuber development and metabolism. Plasma membrane intrinsic proteins (PIPs) represent the main channel that mediates the efficient water transport across the cell membrane. This study presents the characterization of CePIP2;1, a PIP gene highly abundant in tigernut tubers. This gene with three introns was shown to encode 288 amino acids with the theoretical molecular weight of 30.34 kDa, the isoelectric point of 8.60, the grand average of hydropathicity of 0.529, and the instability index of 29.60, implying it’s stable, basic and hydrophobic characteristics. The protein was shown to possess one conservative MIP (major intrinsic protein) domain, and presence of the F-H-T-R ar/R selectivity filter and Q-S-A-F-W Froger’s positions implies a putatively efficient water transport activity. Phylogenetic analysis revealed that CePIP2;1 clusters with OsPIP2;1, OsPIP2;2, and OsPIP2;3 with the similarities of 91.72%, 90.31% and 84.98%, respectively, supporting its assignment into the PIP2 group of the PIP subfamily. Subcellular localization analysis showed that CePIP2;1 was localized to the cell membrane of Nicotiana benthamiana leaves. Although CePIP2;1 was characterized as a dominant isoform in tubers, expression analysis indicated that its transcripts were relatively more in leaves, leaf sheaths, rhizomes, and roots with the most in leaves, in contrast to a comparable level to that in shoot apexes. Among four typical stages (S1–S4) of tuber development examined in this study, CePIP2;1 was shown to exhibit a bell-shaped expression pattern, peaking at S2. These results laid a solid foundation for further uncovering the mechanism of water balance in tigernut.

, authors=null, authorsList=Zhi ZOU, Yujiao ZHENG, Lili CHANG, Yongguo ZHAO, authorCompany=null, correspAuthors=null, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, 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, fund=null), CN=ArticleExt(id=1276597976797679989, articleId=1276597973786169707, tenantId=1146029695717560320, journalId=1235980609244409860, language=CN, title=油莎豆CePIP2;1的克隆、亚细胞定位与表达分析, columnId=1236256430517440904, journalTitle=热带作物学报, columnName=组学与生物技术, runingTitle=null, highlight=null, articleAbstract=

油莎豆是一种在块茎中高水平积累油脂的草本油料作物，其未成熟块茎的含水量高达85%，水分平衡对于块茎的发育与代谢至关重要。质膜内在蛋白（PIP）是介导细胞间水分跨膜运输的主要通道。本研究报道1个块茎高水平表达的PIP基因CePIP2；1，该基因含有3个内含子，预测编码288个氨基酸（aa），其理论分子量（MW）为30.34 kDa，等电点（pI）为8.60，总平均疏水指数（GRAVY）为0.529，不稳定系数（Ⅱ）为29.60，属于典型的稳定、碱性、疏水型蛋白。CePIP2；1含有保守的MIP结构域，ar/R选择性滤器为F-H-T-R，Froger位点为Q-S-A-F-W，符合高水分转运活性PIP的特征。进化分析显示，CePIP2；1与OsPIP2；1、OsPIP2；2和OsPIP2；3聚在一起，序列相似性分别为91.72%、90.31%和84.98%，支持其归为PIP2亚类。亚细胞定位分析显示，CePIP2；1定位在烟草叶片的细胞膜。进一步的表达分析显示，虽然CePIP2；1为主要的块茎表达PIP基因，但其在叶片、叶鞘、匍匐茎和根等组织中的表达丰度更高，最高的为叶片，而在芽尖中的表达丰度与块茎相当；在块茎的4个典型发育时期（S1~S4）中，CePIP2；1基因呈现先升后降的钟形趋势，表达丰度最高的是S2。这些结果为解析油莎豆的水分平衡机制奠定基础。

, authors=

邹智（1982—），男，硕士，研究员，研究方向：基因组进化与油脂调控；E-mail：。

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邹智（1982—），男，硕士，研究员，研究方向：基因组进化与油脂调控；E-mail：。

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邹智（1982—），男，硕士，研究员，研究方向：基因组进化与油脂调控；E-mail：。

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Proceedings of the National Academy of Sciences, 2007, 104(30): 12359-12364., articleTitle=FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization, refAbstract=null), Reference(id=1276598265168663268, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, doi=null, pmid=null, pmcid=null, year=2022, volume=112, issue=2, pageStart=518, pageEnd=534, url=null, language=null, rfNumber=[30], rfOrder=35, authorNames=NIEMEYER P W, IRISARRI I, SCHOLZ P, SCHMITT K, VALERIUS O, BRAUS G H, HERRFURTH C, FEUSSNER I, SHARMA S, CARLSSON A S, DE VRIES J, HOFVANDER P, ISCHEBECK T, journalName=Plant Journal, refType=null, unstructuredReference=NIEMEYER P W, IRISARRI I, SCHOLZ P, SCHMITT K, VALERIUS O, BRAUS G H, HERRFURTH C, FEUSSNER I, SHARMA S, CARLSSON A S, DE VRIES J, HOFVANDER P, ISCHEBECK T. A seed-like proteome in oil-rich tubers[J]. Plant Journal, 2022, 112(2): 518-534., articleTitle=A seed-like proteome in oil-rich tubers, refAbstract=null)], funds=[Fund(id=1276598259342774970, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, awardId=ZDYF2024XDNY171, language=CN, fundingSource=海南省重点研发计划项目(ZDYF2024XDNY171), fundOrder=null, country=null), Fund(id=1276598259644764859, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, awardId=SCKJ-JYRC-2022-66, language=CN, fundingSource=“崖州湾”菁英人才科技专项(SCKJ-JYRC-2022-66), fundOrder=null, country=null), Fund(id=1276598260060000956, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, awardId=31971688, language=CN, fundingSource=国家自然科学基金项目(31971688), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1276598246764057223, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, xref=null, ext=[AuthorCompanyExt(id=1276598246780834440, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, companyId=1276598246764057223, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=National Key Laboratory for Tropical Crop Breeding / Institute of Tropical Biosciences and Biotechnology, Chinese Academy of Tropical Agricultural Sciences / Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan 571101, China), AuthorCompanyExt(id=1276598246797611657, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, companyId=1276598246764057223, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=热带作物生物育种全国重点实验室/中国热带农业科学院热带生物技术研究所/中国热带农业科学院三亚研究院，海南海口　571101)])], figs=[ArticleFig(id=1276598255140082349, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=EN, label=Fig. 1, caption=Bioinformatics analysis of CePIP2;1

A: Gene structure of CePIP2;1; B: Comparison of amino acid composition of CePIP2;1, SoPIP2;1, AtPIP2;1 and AtPIP2;4; C: Predicted conservative domain of CePIP2;1; D: Multiple sequence alignment of CePIP2;1, SoPIP2;1, AtPIP2;1 and AtPIP2;4; E: Phylogenetic analysis of CePIP2;1, SoPIP2;1, and PIPs present in O. sativa and A. thaliana; F: Predicted 3D structure for CePIP2;1.

, figureFileSmall=6k89VgLDauakNApyVzyGiA==, figureFileBig=I0p2BuNrGwdtzdDnxZUwYg==, tableContent=null), ArticleFig(id=1276598255207191214, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=CN, label=图1, caption=CePIP2;1的生物信息学分析

A：CePIP2;1的基因结构；B：CePIP2;1与SoPIP2;1、AtPIP2;1、AtPIP2;4的氨基酸组成比较；C：CePIP2;1的保守结构域预测；D：CePIP2;1与SoPIP2;1、AtPIP2;1、AtPIP2;4的多序列比对；E：CePIP2;1与SoPIP2;1、水稻、拟南芥中的PIP蛋白的进化分析；F：CePIP2;1的3D结构预测。

, figureFileSmall=6k89VgLDauakNApyVzyGiA==, figureFileBig=I0p2BuNrGwdtzdDnxZUwYg==, tableContent=null), ArticleFig(id=1276598255551124143, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=EN, label=Fig. 2, caption=Subcellular localization analysis of CePIP2;1, figureFileSmall=rfiwWsq5sOcFqdYcoOpNwA==, figureFileBig=D9d5DhpeRssC87xiktG34A==, tableContent=null), ArticleFig(id=1276598255874085552, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=CN, label=图2, caption=CePIP2;1的亚细胞定位, figureFileSmall=rfiwWsq5sOcFqdYcoOpNwA==, figureFileBig=D9d5DhpeRssC87xiktG34A==, tableContent=null), ArticleFig(id=1276598255953777329, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=EN, label=Fig. 3, caption=Expression profiles of CePIP2;1

Different capital letters indicate extremely significant difference (P<0.01).

, figureFileSmall=+y/00MJDCd9GOHtMqwhQyw==, figureFileBig=OxR2p+WgqhphTvDylfgb7Q==, tableContent=null), ArticleFig(id=1276598256020886194, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=CN, label=图3, caption=CePIP2;1的表达模式

不同大写字母表示差异极显著（P<0.01）。

, figureFileSmall=+y/00MJDCd9GOHtMqwhQyw==, figureFileBig=OxR2p+WgqhphTvDylfgb7Q==, tableContent=null), ArticleFig(id=1276598256356430515, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=EN, label=Tab. 1, caption=

Databases, software and related websites used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
数据库/软件Database/software网址Website用途Application
Araport11https://www.arabidopsis.org/拟南芥PIP基因下载
RGAP7http://rice.plantbiology.msu.edu/水稻PIP基因下载
CNGBdbhttps://db.cngb.org/search/assembly/CNA0051961/油莎豆基因组数据下载
NCBIhttps://www.ncbi.nlm.nih.gov/转录组数据和PIP基因下载
BLASThttps://blast.ncbi.nlm.nih.gov/Blast.cgi核苷酸和蛋白序列比对
StringTiehttps://ccb.jhu.edu/software/stringtie/转录组数据的比对
GSDS2.0http://gsds.gao-lab.org/基因结构展示
ProtParamhttps://web.expasy.org/protparam/蛋白理化特性分析
WoLF PSORThttps://www.genscript.com/wolf-psort.html亚细胞定位预测
CDDhttps://www.ncbi.nlm.nih.gov/cdd保守结构域预测
SOPMAhttps://npsa-prabi.ibcp.fr/cgi-bin/npsa_automat.pl?page=/NPSA/npsa_sopma.html二级结构预测
SWISS-MODELhttps://swissmodel.expasy.org/interactive3D结构预测
MEGA6.06https://mega6.software.informer.com/多序列比对和进化树的构建
), ArticleFig(id=1276598256469676724, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=CN, label=表1, caption=

研究所用数据库、软件及其网址

, figureFileSmall=null, figureFileBig=null, tableContent=
数据库/软件Database/software网址Website用途Application
Araport11https://www.arabidopsis.org/拟南芥PIP基因下载
RGAP7http://rice.plantbiology.msu.edu/水稻PIP基因下载
CNGBdbhttps://db.cngb.org/search/assembly/CNA0051961/油莎豆基因组数据下载
NCBIhttps://www.ncbi.nlm.nih.gov/转录组数据和PIP基因下载
BLASThttps://blast.ncbi.nlm.nih.gov/Blast.cgi核苷酸和蛋白序列比对
StringTiehttps://ccb.jhu.edu/software/stringtie/转录组数据的比对
GSDS2.0http://gsds.gao-lab.org/基因结构展示
ProtParamhttps://web.expasy.org/protparam/蛋白理化特性分析
WoLF PSORThttps://www.genscript.com/wolf-psort.html亚细胞定位预测
CDDhttps://www.ncbi.nlm.nih.gov/cdd保守结构域预测
SOPMAhttps://npsa-prabi.ibcp.fr/cgi-bin/npsa_automat.pl?page=/NPSA/npsa_sopma.html二级结构预测
SWISS-MODELhttps://swissmodel.expasy.org/interactive3D结构预测
MEGA6.06https://mega6.software.informer.com/多序列比对和进化树的构建
), ArticleFig(id=1276598258399056565, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=EN, label=Tab. 2, caption=

Primers used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
引物名称Primer name引物序列（5'–3'）Primer sequence (5'–3')
CePIP2;1FCACACATCACTCTTTGCTCT
CePIP2;1RGCGAGCAACAGAGACTACTA
CePIP2;1HFAGTGGTCTCTGTCCAGTCCTATGTCCAAGGAGGTGAGTGAGG
CePIP2;1HRGGTCTCAGCAGACCACAAGTTTACGCATTGCTGCGGAAC
CeUCE2FqATCATCAAGGAGACCCAGCG
CeUCE2RqCTTAGGGGCAGCCATAGGA
CeTIP41FqCGGCGAGCGACCTGAA
CeTIP41RqCAGCGGCAGAGTTGAGAATG
CePIP2;1FqGGTGCCATTTGCGGTGTC
CePIP2;1RqCCCTTGAGTAGCCGTGTGC
), ArticleFig(id=1276598258474554038, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=CN, label=表2, caption=

研究所用引物

, figureFileSmall=null, figureFileBig=null, tableContent=
引物名称Primer name引物序列（5'–3'）Primer sequence (5'–3')
CePIP2;1FCACACATCACTCTTTGCTCT
CePIP2;1RGCGAGCAACAGAGACTACTA
CePIP2;1HFAGTGGTCTCTGTCCAGTCCTATGTCCAAGGAGGTGAGTGAGG
CePIP2;1HRGGTCTCAGCAGACCACAAGTTTACGCATTGCTGCGGAAC
CeUCE2FqATCATCAAGGAGACCCAGCG
CeUCE2RqCTTAGGGGCAGCCATAGGA
CeTIP41FqCGGCGAGCGACCTGAA
CeTIP41RqCAGCGGCAGAGTTGAGAATG
CePIP2;1FqGGTGCCATTTGCGGTGTC
CePIP2;1RqCCCTTGAGTAGCCGTGTGC
), ArticleFig(id=1276598258554245815, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=EN, label=Tab. 3, caption=

Comparison of physicochemical properties and secondary structure of CePIP2;1, SoPIP2;1, AtPIP2;1 and AtPIP2;4

, figureFileSmall=null, figureFileBig=null, tableContent=
蛋白名称Protein nameAAMW/kDapIGRAVYAIIIMIPα-螺旋Alpha helix/%延伸链Extended strand/%β-转角Beta turn/%无规则卷曲Random coil/%
CePIP2;128830.348.600.529103.0229.6032~26929.5120.834.1745.49
SoPIP2;128129.909.030.579102.8127.8131~26036.6518.152.1443.06
AtPIP2;128730.478.600.50697.9430.2730~26640.4216.724.8837.98
AtPIP2;429130.958.220.49096.2929.2930~26630.2420.965.1543.64
), ArticleFig(id=1276598258944316089, tenantId=1146029695717560320, journalId=1235980609244409860, articleId=1276597973786169707, language=CN, label=表3, caption=

CePIP2;1与SoPIP2;1、AtPIP2;1、AtPIP2;4理化特性和二级结构比较

, figureFileSmall=null, figureFileBig=null, tableContent=
蛋白名称Protein nameAAMW/kDapIGRAVYAIIIMIPα-螺旋Alpha helix/%延伸链Extended strand/%β-转角Beta turn/%无规则卷曲Random coil/%
CePIP2;128830.348.600.529103.0229.6032~26929.5120.834.1745.49
SoPIP2;128129.909.030.579102.8127.8131~26036.6518.152.1443.06
AtPIP2;128730.478.600.50697.9430.2730~26640.4216.724.8837.98
AtPIP2;429130.958.220.49096.2929.2930~26630.2420.965.1543.64
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油莎豆CePIP2;1的克隆、亚细胞定位与表达分析
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邹智 , 郑玉皎 , 常丽丽 , 赵永国
热带作物学报 | 组学与生物技术 2024,45(7): 1340-1347
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热带作物学报 |组学与生物技术 2024 , 45 (7) : 1340 -1347
油莎豆CePIP2;1的克隆、亚细胞定位与表达分析
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邹智 , 郑玉皎, 常丽丽, 赵永国
作者信息
  • 热带作物生物育种全国重点实验室/中国热带农业科学院热带生物技术研究所/中国热带农业科学院三亚研究院，海南海口　571101
Cloning, Subcellular Localization, and Expression Analysis of CePIP2;1, an Aquaporin Gene from Tigernut (Cyperus esculentus L.)
Zhi ZOU , Yujiao ZHENG, Lili CHANG, Yongguo ZHAO
Affiliations
  • National Key Laboratory for Tropical Crop Breeding / Institute of Tropical Biosciences and Biotechnology, Chinese Academy of Tropical Agricultural Sciences / Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan 571101, China
出版时间: 2024-07-25 doi: 10.3969/j.issn.1000-2561.2024.07.005
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油莎豆是一种在块茎中高水平积累油脂的草本油料作物，其未成熟块茎的含水量高达85%，水分平衡对于块茎的发育与代谢至关重要。质膜内在蛋白（PIP）是介导细胞间水分跨膜运输的主要通道。本研究报道1个块茎高水平表达的PIP基因CePIP2；1，该基因含有3个内含子，预测编码288个氨基酸（aa），其理论分子量（MW）为30.34 kDa，等电点（pI）为8.60，总平均疏水指数（GRAVY）为0.529，不稳定系数（Ⅱ）为29.60，属于典型的稳定、碱性、疏水型蛋白。CePIP2；1含有保守的MIP结构域，ar/R选择性滤器为F-H-T-R，Froger位点为Q-S-A-F-W，符合高水分转运活性PIP的特征。进化分析显示，CePIP2；1与OsPIP2；1、OsPIP2；2和OsPIP2；3聚在一起，序列相似性分别为91.72%、90.31%和84.98%，支持其归为PIP2亚类。亚细胞定位分析显示，CePIP2；1定位在烟草叶片的细胞膜。进一步的表达分析显示，虽然CePIP2；1为主要的块茎表达PIP基因，但其在叶片、叶鞘、匍匐茎和根等组织中的表达丰度更高，最高的为叶片，而在芽尖中的表达丰度与块茎相当；在块茎的4个典型发育时期（S1~S4）中，CePIP2；1基因呈现先升后降的钟形趋势，表达丰度最高的是S2。这些结果为解析油莎豆的水分平衡机制奠定基础。

油料作物  /  块茎  /  水通道蛋白  /  质膜内在蛋白  /  亚细胞定位  /  表达模式

Tigernut (Cyperus esculentus L.) is an herbaceous oil crop uniquely accumulating a high level of oil in the underground tubers. Water, which accounts for approximately 85% of immature tubers, is essential for tuber development and metabolism. Plasma membrane intrinsic proteins (PIPs) represent the main channel that mediates the efficient water transport across the cell membrane. This study presents the characterization of CePIP2;1, a PIP gene highly abundant in tigernut tubers. This gene with three introns was shown to encode 288 amino acids with the theoretical molecular weight of 30.34 kDa, the isoelectric point of 8.60, the grand average of hydropathicity of 0.529, and the instability index of 29.60, implying it’s stable, basic and hydrophobic characteristics. The protein was shown to possess one conservative MIP (major intrinsic protein) domain, and presence of the F-H-T-R ar/R selectivity filter and Q-S-A-F-W Froger’s positions implies a putatively efficient water transport activity. Phylogenetic analysis revealed that CePIP2;1 clusters with OsPIP2;1, OsPIP2;2, and OsPIP2;3 with the similarities of 91.72%, 90.31% and 84.98%, respectively, supporting its assignment into the PIP2 group of the PIP subfamily. Subcellular localization analysis showed that CePIP2;1 was localized to the cell membrane of Nicotiana benthamiana leaves. Although CePIP2;1 was characterized as a dominant isoform in tubers, expression analysis indicated that its transcripts were relatively more in leaves, leaf sheaths, rhizomes, and roots with the most in leaves, in contrast to a comparable level to that in shoot apexes. Among four typical stages (S1–S4) of tuber development examined in this study, CePIP2;1 was shown to exhibit a bell-shaped expression pattern, peaking at S2. These results laid a solid foundation for further uncovering the mechanism of water balance in tigernut.

oil crop  /  tuber  /  aquaporin  /  plasma membrane intrinsic protein  /  subcellular localization  /  expression profile
邹智, 郑玉皎, 常丽丽, 赵永国. 油莎豆CePIP2;1的克隆、亚细胞定位与表达分析. 热带作物学报, 2024 , 45 (7) : 1340 -1347 . DOI: 10.3969/j.issn.1000-2561.2024.07.005
Zhi ZOU, Yujiao ZHENG, Lili CHANG, Yongguo ZHAO. Cloning, Subcellular Localization, and Expression Analysis of CePIP2;1, an Aquaporin Gene from Tigernut (Cyperus esculentus L.)[J]. Chinese Journal of Tropical Crops, 2024 , 45 (7) : 1340 -1347 . DOI: 10.3969/j.issn.1000-2561.2024.07.005
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质膜内在蛋白（plasma membrane intrinsic protein，PIP）隶属于水通道蛋白（aquaporin，AQP）家族，其以定位在细胞膜且具有高效的水分转运活性而著称[1]。除水分外，PIP还可以转运尿素、硼酸、CO2、H2O2、O2和Na+[2]。在高等植物中，PIP亚族的成员数介于2~28个不等，可以分为PIP1和PIP2两个进化小组[3-9]。目前晶体结构已解析的有菠菜（Spinacia oleracea）PIP2;1、拟南芥（Arabidopsis thaliana）PIP2;1（PIP2或PIP2A）和AtPIP2;4（PIP2F）[10-12]。研究表明，PIP在细胞膜上以四聚体的形式起作用，每个单体包含6个跨膜螺旋（TM1~TM6）和5个连环（LA、LB、LC、LD和LE），其中，LB、LD、N端和C端位于胞质，而LA、LC和LE位于胞外；LB和LE折向膜内形成2个半螺旋，半螺旋的顶端含有高度保守的NPA基序，起排斥质子并决定通道大小的作用；位于TM2、TM5和LE上的4个保守残基（H2、H5、LE1和LE2）决定了底物特异性，因H2和LE2分别为芳香氨基酸和精氨酸而被称为ar/R选择性滤器[10]。此外，FROGER等[13]从甘油通道蛋白（glyceroporin，GLP）中鉴定到区别于AQP的5个残基，即P1为芳香氨基酸、P2为酸性氨基酸、P3为碱性氨基酸、P4为脯氨酸以及P5为非芳香氨基酸。除转录外，PIP还受翻译后修饰（如磷酸化、甲基化、乙酰化、泛素化、糖基化、脱酰胺基）、二聚化、转运、门控（如二价阳离子、pH、磷酸化）和蛋白互作等调控[10-11,14]。位于SoPIP2;1 LA的C69为二聚体的形成所必须；位于LD的H193和L197为门控位点；位于LB的S115、LD的S188以及位于C端的S274为门控调控磷酸化位点[10]。
油莎豆（Cyperus esculentus L.），俗称黄色道格拉斯（yellow nutsedge）、虎坚果（tigernut），是一种隶属于禾本目莎草科的新型草本油料作物[15-19]。不同于传统油料作物在种子中积累油脂，油莎豆是迄今唯一已知在块茎中高水平积累油脂的作物，这使其成为研究营养组织油脂代谢与调控的模式[20-23]。块茎起源于地下匍匐茎，其发育过程可分为起始、膨大和成熟等3个主要阶段；前2个阶段的含水量高达85%，而在成熟期发生类似种子的脱水过程，含水量逐渐降低到45%以下[17,20]。水分平衡对于块茎的发育乃至油脂和淀粉等储藏物的积累至关重要[20]，因而挖掘块茎中的关键PIP基因具有重要的理论意义和应用价值。本研究对1个块茎高水平表达的PIP基因进行了克隆和初步鉴定，以期为揭示块茎的水分平衡机制奠定基础。
1　材料与方法
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1.1　材料
研究所用油莎豆品系为热研3号，植株种植于中国热带农业科学院文昌实验基地[21]，待块茎起始后分别采集1 d（起始期，S1）、20 d（膨大中期，S2）、25 d（膨大晚期，S3）和35 d（成熟期，S4）的样本，每样本3次生物学重复。本氏烟草（Nicotiana benthamiana）用小钵种在中国热带农业科学院热带生物技术研究所温室[24]。大肠杆菌（Escherichia coli）DH5α和含pSoup-P19的农杆菌（Agrobacterium tumefaciens）GV3101感受态均由本实验室制备和保存；亚细胞定位载体pNC-HbPIP2;3-RFP[25]和pNC-Cam1304-SubN由本实验室保存；各类酶、试剂盒和生化试剂购自相应的试剂公司。本研究所用数据库、软件及其网址详见表1。
1.2　方法
1.2.1　总RNA的提取与反转录
采用天根植物多糖多酚RNA提取试剂盒提取上述块茎的总RNA，经浓度和完整性检测合格后用赛默飞反转录试剂盒合成cDNA第一链，用于后续的基因克隆与表达分析。
1.2.2　基因克隆与载体构建
前期通过分析油莎豆的转录组数据[21]，发现1个在块茎中高水平表达的PIP基因，根据序列特征和进化关系将其命名为CePIP2;1。为克隆该基因，采用Primer Premier 5.0设计如表2所示的引物对，首先用CePIP2;1F/R扩增其1127 bp的全长cDNA，接着以稀释100倍的首轮PCR产物作为模板、CePIP2;1HF/R为引物扩增907 bp的全长编码区（CDS）。反应体系：模板0.5 μL、引物各0.5 μL、PrimeSTAR Max DNA Polymerase 12.5 μL，加ddH2O至25 μL。PCR扩增程序：95 ℃预变性1 min；94 ℃变性30 s、50 ℃退火2 min，35个循环；72 ℃延伸5 min。亚细胞定位载体pNC-Cam1304-CePIP2;1的构建参照NC克隆试剂盒说明书。
1.2.3　基因和蛋白结构分析
采用BLASTn将基因的转录本序列比对到基因组，然后用GSDS 2.0软件展示基因结构。分别采用Protparam、CDD、SOPMA、SWISS-MODEL、WoLF PSORT等软件分析CePIP2;1编码蛋白的理化特性、保守结构域、二级结构、3D结构和亚细胞定位。跨膜螺旋和半螺旋区及保守氨基酸基于与SoPIP2;1、AtPIP2;1和AtPIP2;4的序列比对进行确定。
1.2.4　多序列比对和进化分析
多序列比对采用MUSCLE软件，选用默认参数；进化树的构建采用MEGA 6.06软件，选用最大似然法，1000次重复，其他用默认参数。
1.2.5　亚细胞定位分析
以先前报道的pNC-HbPIP2;3-RFP[25]为阳性对照，参照文献[24]进行农杆菌的转化、培养及浸染液的制备。将含pNC-Cam1304-CePIP2;1的实验组与阳性对照菌液等量混合后采用微量注射器注射4周龄的烟草叶片，转化48 h后用激光共聚焦显微镜Zeiss LMS880观察荧光在细胞内的位置。
1.2.6　基因表达分析
为分析基因的组织特异性，参照文献[23]，采用StringTie（v2.2.0）软件将不同组织的转录组数据（PRJNA703731）比对到基因组，基因的相对表达丰度用FKPM（fragments per kilobase of exon per million fragments mapped）法进行均一化。荧光定量分析以先前报道的CeUCE2和CeTIP41[18]作为内参基因，利用引物对CePIP2;1Fq/Rq进行qRT-PCR分析，数据分析采用2-△△CT法，统计分析采用SPSS 20软件，采用邓肯法进行单因素多样本间差异显著性方差分析。
2　结果与分析
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2.1　 CePIP2;1基因的克隆与序列分析
经过2轮巢式PCR扩增，成功分离到CePIP2;1的CDS序列，并采用无缝克隆技术将其克隆到亚细胞定位载体，构建重组质粒pNC-Cam1304-CePIP2;1。通过将克隆到的序列比对到基因组，发现其与CePIP2;1基因的对应区域完成一致；CePIP2;1位于Scaffold9正向链的879960~884243位，基于转录组的转录区界定显示基因全长为5752 bp，包含3个内含子，其长度分别为806、1745、866 bp；5'和3' UTR分别为119、1349 bp（图1A）。
序列分析显示，CePIP2;1编码288个氨基酸（表3），其中，A和G的含量最高，分别占12.50%和12.20%，这与SoPIP2;1、AtPIP2;1和AtPIP2;4类似（图1B）；CePIP2;1的理论分子量（MW）为30.34 kDa、等电点（pI）为8.60、脂肪族指数（AI）为103.02、总平均疏水指数（GRAVY）为0.529、不稳定系数（Ⅱ）为29.60，表明其为稳定的碱性疏水型蛋白；CDD分析显示蛋白的32~269位为MIP结构域（图1C），略长于SoPIP2;1、AtPIP2;1和AtPIP2;4（表3）；CePIP2;1与SoPIP2;1、AtPIP2;1、AtPIP2;4的序列相似性分别为84.88%、84.14%、84.35%，其结构包括TM1~TM6等6个典型的跨膜螺旋、HB和HE 2个半螺旋、2个典型的NPA基序、多个磷酸化位点（S105、S124、S283和S286）；ar/R选择性滤器（F90-H219-T228-R234）和对应于SoPIP2;1 C69的二聚化位点、S115的磷酸化位点及H193和L197门控位点在所比较的4个蛋白中完全一致；在5个Froger位点中，仅P1存在差异，SoPIP2;1为M141-S226-A230-F245-W246，而CePIP2；1为Q150-S235-A239-F254-W255（图1D）。
为揭示CePIP2;1的进化关系，将其与SoPIP2;1及水稻、拟南芥中的所有PIP构建如图1E所示的进化树。多数成员按物种聚在一起，暗示相关成员在物种分化之后产生。CePIP2;1与OsPIP2;1、OsPIP2;2、OsPIP2;3聚在一起，其序列相似性分别为91.72%、90.31%和84.98%。二级结构预测显示，CePIP2;1以无规则卷曲（45.49%）和α-螺旋为主（29.51%），其次是延伸链（20.83%），最低的为β-转角（4.17%），与SoPIP2;1、AtPIP2;1和AtPIP2;4类似（表3）。基于SoPIP2;1的同源建模显示，CePIP2;1可以形成同源四聚体（图1F）。
2.2　亚细胞定位分析
与其他PIP蛋白类似[24-25]，WoLF PSORT在线软件预测显示CePIP2;1定位在细胞膜。为验证该结果，本研究以先前报道的HbPIP2;3[25]作为阳性对照，将含pNC-HbPIP2;3-RFP和pNC-Cam1304- CePIP2;1的农杆菌工程菌等量混合后微量注射烟草叶片。共聚焦观察结果显示，GFP-CePIP2;1的绿色荧光信号出现在细胞膜，并与HbPIP2;3-RFP的红色荧光信号高度重合，这表明CePIP2;1确实是定位在细胞膜（图2）。
2.3　基因表达分析
为揭示CePIP2;1基因表达的组织特异性，利用转录组数据分析其在幼嫩叶片、成熟叶片、叶鞘、根、匍匐茎、芽尖和块茎等主要组织中的表达模式。结果显示，CePIP2;1在这些组织中均高水平表达，丰度最高的是叶片（幼嫩和成熟叶片差异不显著），最低的为芽尖，其与块茎丰度相当（图3A）。
为揭示基因表达与不同发育时期块茎含水量之间的相关性，挑选自块茎形成起始期（S1）、膨大中期（S2）、膨大晚期（S3）和成熟期（S4）等4个典型时期，其含水量分别为83.7%、86.0%、74.8%和48.3%[17]。qRT-PCR分析结果如图3B所示，CePIP2;1基因呈先升后降的趋势，峰值出现在S2，约为S1的1.5倍；丰度最低的是S4，仅为S1的8%；S3仅为S2的30%。
3　讨论
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水是生命的主要存在形式，广泛参与体内的各项生理生化反应，为植物的生长发育和代谢活动所必需[2]。研究表明，植物细胞间水分的跨膜运输主要由细胞膜定位的PIP介导[1,2]。进化分析显示，PIP高度保守，仅包含PIP1和PIP2两个亚类；虽然他们早在苔藓中就已分化形成，但二者之间的序列相似性一般在70%以上[3-9,26]。PIP通常具有高效的水分转运活性[2]。虽然有研究表明PIP1亚类在酵母和蟾蜍卵母细胞等体外体系中无活性或活性很低，主要归因于其自身不能有效定位到细胞膜[27-28]。在植物体内，PIP2的存在可以介导PIP1的有效定位[27-29]。
在前期的研究中，本团队系统分析了块茎的发育特征及发育过程中的含水动力学，发现在我国海南地区块茎的整个发育期约为35 d，其中，前、中期伴随着细胞的快速分裂和扩张，水分含量一直维持在85%，而后期随着块茎的成熟，水分含量逐步降低，25 d和35 d分别为74.8%和48.3%[17]，发生类似种子的脱水过程[17,30]。虽然如此，至今对油莎豆块茎发育的水分平衡机制知之甚少。
本研究首次报道了1个油莎豆PIP2基因CePIP2;1。与大多数PIP基因类似[3-9],CePIP2;1含有3个内含子；其编码蛋白包含AQP家族特有的MIP结构域，分子量为30.76 kDa，与先前的报道相似[5-9,25-26]。CePIP2;1具有较高的脂肪族指数（95.28），且总平均疏水指数>0、等电点>7.0、不稳定系数为<40，属于典型的稳定、碱性、疏水型蛋白。在水稻的13个PIP蛋白中，CePIP2;1与OsPIP2;1的序列相似性最高（91.72%），略高于与OsPIP2;2的90.31%，但远高于与OsPIP1的72.19%~74.59%，这与本研究的结果一致，支持其划归为PIP2亚类。此外，CePIP2;1具有SoPIP2;1[10]、AtPIP2;1[11]和AtPIP2;4[12]相似的结构特征，其中包括典型的NPA基序、F-H-T-R ar/R选择性滤器、Q-S-A-F-W Froger位点、位于LA高度保守的C残基、可形成四聚体，并且被实验证实定位在烟草叶片的细胞膜，这些均表明CePIP2;1可能具有高效的水分转运活性。虽然CePIP2;1首先是作为1个块茎高丰度PIP基因而被关注，但组织特异性分析显示它在其他组织中的表达丰度更高，暗示其功能的重要性。在块茎的发育过程中，CePIP2;1呈现先升后降的表达模式，即随着细胞的快速分裂和扩张，CePIP2;1的表达迅速上调，至膨大中期达到峰值，而在成熟过程中逐渐下调，这与相应时期的水分含量趋势基本一致[17]。虽然如此，CePIP2;1具体是如何调控块茎及其他组织的水分平衡还有待深入研究，比如门控调控、翻译后修饰、蛋白互作模式以及调控其转录的上游转录因子。
综上，本研究完成了块茎高水平表达CePIP2;1基因的克隆与初步鉴定，明确了其基因结构、序列特征、进化关系、亚细胞定位和表达特性，这为进一步的功能分析及油莎豆遗传改良奠定了坚实的基础。
基金
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  • 海南省重点研发计划项目(ZDYF2024XDNY171)
  • “崖州湾”菁英人才科技专项(SCKJ-JYRC-2022-66)
  • 国家自然科学基金项目(31971688)
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参考文献 引证文献
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2024年第45卷第7期
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doi: 10.3969/j.issn.1000-2561.2024.07.005
  • 接收时间：2023-06-27
  • 首发时间：2026-06-24
  • 出版时间：2024-07-25
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  • 收稿日期：2023-06-27
  • 修回日期：2023-07-18
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海南省重点研发计划项目(ZDYF2024XDNY171)
“崖州湾”菁英人才科技专项(SCKJ-JYRC-2022-66)
国家自然科学基金项目(31971688)
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    热带作物生物育种全国重点实验室/中国热带农业科学院热带生物技术研究所/中国热带农业科学院三亚研究院，海南海口　571101
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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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