哈氏黄瓜NAC转录因子的鉴定及低温表达分析
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摘要
以哈氏黄瓜(Cucumis sativus var. hardwickii)为试验材料,基于全基因组测序结果,利用生物信息学分析方法,鉴定获得77个NAC转录因子,其结构高度保守,序列长度在151～653个氨基酸之间,在7条染色体中呈非均匀分布;理论等电点在4.54～9.10之间;大部分转录因子定位在细胞核和细胞质膜上;系统发生分析显示所有NAC转录因子聚类为6个亚家族,其中亚家族Ⅲ序列结构较为多样性;进化分析发现NAC转录因子存在片段重复和串联重复等复制模式,没有发生近代的全基因组复制事件,并在进化过程中受到纯化选择作用;NAC转录因子基因在哈氏黄瓜幼苗根中表达量最高,其次为雌花和叶片;荧光定量分析发现,低温处理下,检测的15个NAC基因中有12个显著上调表达,3个下调表达,并存在一组表达量差异明显的HdNAC32–Hd ANC47片段复制基因对。由此可知NAC转录因子在受低温胁迫的哈氏黄瓜中发挥重要的转录调控作用。
The hardwickii(Cucumis sativus var. hardwickii)is recognized as the wild ancestor of cultivated cucumber,and plays an important role in cucumber genetics and cultivar improvement. In this study,a total of 77 NAC transcription factors were identified with methods of bioinformatics based on sequencing hardwickii genome. The NAC transcription factors were highly conserved. The length of sequences varied and ranged from 151 to 653 amino acids,and unevenly distributed in seven chromosomes. The theoretical isoelectric point(pI)ranged from 4.54 to 9.10. Most of NAC transcription factors were located in the cell nucleus and plasma membrane. Phylogenetic analysis showed that NAC proteins could be classified into six subfamilies,of which the third subfamily exhibited structural diversity.Evolutionary analysis indicated that segmental and tandem duplication events had occurred under the purifying selection pressure,while no recent whole-genome duplication(WGD)events were found in NAC transcription factors. Tissue-specific expression analysis showed that most of genes were highly expressed in root,followed by the female flowers and leaves. In addition,12 up-regulated NAC genes and 3 down-regulated NAC genes were identified under low temperature treatment via RT-PCR. Among which,HdNAC32 and HdANC47,a pair of segmental duplication genes,showed opposite expression patterns.Thus the conclusion was drawn out that NAC transcription factors play a critical role in the transcriptional regulation of cold tolerance in hardwickii under cold stress.
The hardwickii(Cucumis sativus var. hardwickii)is recognized as the wild ancestor of cultivated cucumber,and plays an important role in cucumber genetics and cultivar improvement. In this study,a total of 77 NAC transcription factors were identified with methods of bioinformatics based on sequencing hardwickii genome. The NAC transcription factors were highly conserved. The length of sequences varied and ranged from 151 to 653 amino acids,and unevenly distributed in seven chromosomes. The theoretical isoelectric point(pI)ranged from 4.54 to 9.10. Most of NAC transcription factors were located in the cell nucleus and plasma membrane. Phylogenetic analysis showed that NAC proteins could be classified into six subfamilies,of which the third subfamily exhibited structural diversity.Evolutionary analysis indicated that segmental and tandem duplication events had occurred under the purifying selection pressure,while no recent whole-genome duplication(WGD)events were found in NAC transcription factors. Tissue-specific expression analysis showed that most of genes were highly expressed in root,followed by the female flowers and leaves. In addition,12 up-regulated NAC genes and 3 down-regulated NAC genes were identified under low temperature treatment via RT-PCR. Among which,HdNAC32 and HdANC47,a pair of segmental duplication genes,showed opposite expression patterns.Thus the conclusion was drawn out that NAC transcription factors play a critical role in the transcriptional regulation of cold tolerance in hardwickii under cold stress.
引文
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Duval M,Hsieh T,Kim S Y,Thomas T L.2002.Molecular characterization of AtNAM:a member of the Arabidopsis NAC domain superfamily.Plant Mol Biol,50:237-248.
Guo W L,Wang S B,Chen R G,Chen B H,Du X H,Yin Y X,Gong Z H,Zhang Y Y.2015.Characterization and expression profile of CaNAC2pepper gene.Frontiers in Plant Science,6:755.
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Hussey S G,Mizrachi E,Spokevicius A V,Bossinger G,Berger D K,Myburg A A.2011.SND2,a NAC transcription factor gene,regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus.BMC Biology,11:173.
Kikuchi K,Ueguchi-Tanaka M,Yoshida T K,Nagato Y,Matsusoka M,Hirano H Y.2000.Molecular analysis of the NAC gene family in rice.Mol Gen Genet,262:1047-1051.
Krzywinski M,Schein J,Birol I,Connors J,Gascoyne R,Horsman D,Jones S J,Marra M A.2009.Circos:an information aesthetic for comparative genomics.Genome Research,19:1639-1645.
Kumar S,Stecher G,Tamura K.2015.MEGA7:Molecular evolutionary genetics analysis version 7.0.Molecular Biology and Evolution,33(7):1870-1874.
Le D T,Nishiyama R,Watanabe Y,Mochida K,Yamaguchi-Shinozaki K,Shinozaki K,Tran L S P.2011.Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress.DNA Research,18:263-276.
Lin De-pei.2017.A study of origin and taxonomy on cucumber.China Cucurbits and Vegetables,30(7):1-3.(in Chinese)林德佩.2017.黄瓜植物的起源和分类研究进展.中国瓜菜，30(7):1-3.
Lin R M,Zhao W S,Meng X B,Wang M,Peng Y L.2007.Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea.Plant Science,172:120-130.
Lin Yong-xiang.2013.Molecular evolution of heat shock transcription factor gene families in legumes and grasses[Ph.D.Dissertation].Hefei:Anhui Agricultural University.(in Chinese)林勇翔.2013.豆科和禾本科植物热激转录因子基因家族的分子进化研究[博士论文].合肥：安徽农业大学.
Livak K J,Schmittgen T D.2007.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method.Methods,25(5):402-408.
Lynch M,Conery J S.2000.The evolutionary fate and consequences of duplicate genes.Science,290(5494):1151-1155.
McDonald J H,Kreitman M.1991.Adaptive protein evolution at the Adh locus in Drosophila.Nature,352(6328):652-654.
Ooka H,Satoh K,Doi K,Nagata T,Otomo Y,Murakami K,Matsubara K,Osato N,Kawai J,Carninci P,Hayashizaki Y,Suzuki K,Kojima K,Takahara Y,Yamamoto K,Kikuchi S.2003.Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana.DNAResearch,10:239-247.
Qi J J,Liu X,Shen D,Miao H,Xie B Y,Li X X,Zeng P,Wang S H,Shang Y,Gu X F,Du T C,Li Y,Lin T,Yuan J H,Yang X Y,Chen JF,Chen H M,Xiong X Y,Huang K,Fei Z J,Mao L Y,Tian L,Stadler T,Renner S S,Kamoun S,Lucas W J,Zhang Z H,Huang S W.2013.A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity.Nature Genetics,45:12.
Qiao X,Li M,Li L T,Yin H,Wu J Y,Zhang S L.2015.Genome-wide identification and comparative analysis of the heat shock transcription factor family in Chinese white pear(Pyrus bretschneideri)and five other Rosaceae species.BMC Plant Biology,15:12.
Seo P J,Kim M J,Park J Y,Kim S Y,Jeon J,Lee Y H,Kim J,Park C M.2010a.Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis.The Plant Journal,61:661-671.
Seo P J,Kim M J,Song J S,Kim Y S,Kim H J,Park C M.2010b.Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced change in membrane fluidity.Biochemical Society,427:359-367.
Shang Q M,Li L,Dong C J.2012.Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis satives L.Planta,236:1093-1105.
Wang Y P,Tang H B,DeBarry J D,Tan X,Li J P,Wang X Y,Lee T,Jin H Z,Marler B,Guo H,Kissinger J C,Paterson A H.2012.MCScanX:a toolkit for detection and evolutionary analysis of gene synteny and collinearity.Nucleic Acides Research,40(7):e49.
Wang Y P,Wang X Y,Tang H B,Tan X,Ficklin S P,Feltus F A,Paterson A H.2011.Modes of gene duplication contribute differently to genetic novelty and redundancy,but show parallels across divergent angiosperms.PLoS ONE,6(12):e28150.
Waterhouse A,Bertoni M,Bienert S,Studer G,Tauriello G,Gumienny R,Heer F T,Beer T A P,Rempfer C,Bordoli L,Lepore R,Schwede T.2018.SWISS-MODEL:homology modeling of protein structures and complexes.Nucleic Acides Research,1-8.
Wei S W,Gao L G,Zhang Y D,Zhang F R,Yang X,Huang D F.2016.Genome-wide investigation of the NAC transcription factor family in melon(Cucumis melo L.)and their expression analysis under salt stress.Plant Cell Rep,35:1827-1839.
Yang Z.1998.Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution.Mol Biol Evol,15(5):568-73.
Yang Z H.2007.PAML 4:phylogenetic analysis by maximum likelihood.Mol Biol Evol,24(8):1586-1591.
Yang Z,Nielsen R.2002.Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages.Mol Biol Evol,19(6):908-917.
Yu C S,Lin C J,Hwang J K.2004.Predicting subcellular localization of proteins for gram-negative bacteria by support vector machines based on N-peptide composite-ons.Protein Science,13(6):1402-1406.
Zhang X M,Yu H J,Sun C,Deng J,Zhang X,Liu P,Li Y Y,Li Q,Jiang W J.2017.Genome-wide characterization and expression profiling of the NAC genes under abiotic stresses in Cucumis sativus.Plant Physicalogy and Biochemistry,113:98-109.
Zhu M K,Chen G P,Zhang J L,Zhang Y J,Xie Q L,Zhao Z P,Pan Y,Hu Z L.2014.The abiotic stress-responsive NAC-type transcription factor SINAC4 regulates salt and drought tolerance and stress-related genes in tomato(Solanum lycopersicum).Plant Cell Rep,33:1851-1863.
Apweiler R,Attwood T K,Bairoch A,Bateman A,Birney E,Biswas M,Bucher P,Cerutti L,Corpet F,Croning M D R,Durbin R,Falquet L,Fleischmann W,Gouzy J,Hermjakob H,Hulo N,Jonassen I,Kahn D,Kanapin A,Karavidopoulou Y,Lopez R,Marx B,Mulder N J,Oinn T M,Pagni M,Servant F,Sigrist C J A,Zdobnov E M.2001.The InterPro database:an integrated documentation resource for protein families domains and functional sites.Nucleic Acids Res,29:37-40.
Bailey T L,Boden M,Buske F A,Firth M,Grant C E,Clementi L,Ren J Y,Li W W,Noble W S.2009.MEME SUITE:tools for motif discovery and searching.Nucleic Acids Research,34(2):W369-W373.
Bu Q Y,Jiang H J,Li C B,Zhai Q Z,Zhang J,Wu X Y,Sun J Q,Xie Q,Li C Y.2008.Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses.Cell Research,18:756-767.
Duval M,Hsieh T,Kim S Y,Thomas T L.2002.Molecular characterization of AtNAM:a member of the Arabidopsis NAC domain superfamily.Plant Mol Biol,50:237-248.
Guo W L,Wang S B,Chen R G,Chen B H,Du X H,Yin Y X,Gong Z H,Zhang Y Y.2015.Characterization and expression profile of CaNAC2pepper gene.Frontiers in Plant Science,6:755.
Hong Y B,Zhang H J,Huang L,Li D Y,Song F M.2016.Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice.Frontiers in Plant Science,7:4.
Hu B,Jin J P,Guo A Y,Zhang H,Lou C J,Gao G.2015.GSDS 2.0:an upgraded gene feature visualization server.Bioinformatics,31(2):1296-1297.
Hu H H,You J,Fang Y J,Zhu X Y,Qi Z Y,Xiong L Z.2008.Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice.Plant Mol Biol,67:169-181.
Huang G H,Qu Y,Li T,Yuan H,Wang A D,Tan D M.2018.Comparative transcriptome analysis of Actinidia arguta fruits reveals the involvement of various transcription factors in ripening.Horticultural Plant Journal,4(1):35-42.
Huang S W,Li R Q,Zhang Z H,Li L,Gu X F,Fan W,Lucas W J,Wang X W,Xie B Y,Ni P X,Ren Y Y,Zhu H M,Li J,Lin K,Jin W W,Fei Z J,Li J C,Staub J,Kilian A,Vossen E A G,Wu Y,Guo J,He J,Jia Z Q,Ren Y,Tian G,Lu Y,Ruan J,Qian W B,Wang M W,Huang Q F,Li B,Xuan Z L,Cao J J,Asan,Wu Z G,Zhang J B,Cai G L,Bai Y Q,Zhao B W,Han Y H,Li Y,Li X F,Wang S H,Shi Q X,Liu S Q,Cho W K,Kim J Y,Xu Y,Heller-Uszynska K,Miao H,Cheng Z C,Zhang S P,Wu J,Yang Y H,Kang H X,Li M,Liang H Q,Ren X L,Shi Z B,Wen M,Jian M,Yang H L,Zhang G J,Yang Z T,Chen R,Liu S F,Li J W,Ma L J,Liu H,Zhou Y,Zhao J,Fang X D,Li G Q,Fang L,Li Y R,Liu D Y,Zheng H K,Zhang Y,Qin N,Li Z,Yang G H,Yang H M,Wang J,Sun R F,Zhang B X,Jiang S Z,Wang J,Du Y C,Li S G.2009.The genome of the cucumber,Cucumis sativus L.Nature Genetics,41:1275-1281.
Hussey S G,Mizrachi E,Spokevicius A V,Bossinger G,Berger D K,Myburg A A.2011.SND2,a NAC transcription factor gene,regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus.BMC Biology,11:173.
Kikuchi K,Ueguchi-Tanaka M,Yoshida T K,Nagato Y,Matsusoka M,Hirano H Y.2000.Molecular analysis of the NAC gene family in rice.Mol Gen Genet,262:1047-1051.
Krzywinski M,Schein J,Birol I,Connors J,Gascoyne R,Horsman D,Jones S J,Marra M A.2009.Circos:an information aesthetic for comparative genomics.Genome Research,19:1639-1645.
Kumar S,Stecher G,Tamura K.2015.MEGA7:Molecular evolutionary genetics analysis version 7.0.Molecular Biology and Evolution,33(7):1870-1874.
Le D T,Nishiyama R,Watanabe Y,Mochida K,Yamaguchi-Shinozaki K,Shinozaki K,Tran L S P.2011.Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress.DNA Research,18:263-276.
Lin De-pei.2017.A study of origin and taxonomy on cucumber.China Cucurbits and Vegetables,30(7):1-3.(in Chinese)林德佩.2017.黄瓜植物的起源和分类研究进展.中国瓜菜，30(7):1-3.
Lin R M,Zhao W S,Meng X B,Wang M,Peng Y L.2007.Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea.Plant Science,172:120-130.
Lin Yong-xiang.2013.Molecular evolution of heat shock transcription factor gene families in legumes and grasses[Ph.D.Dissertation].Hefei:Anhui Agricultural University.(in Chinese)林勇翔.2013.豆科和禾本科植物热激转录因子基因家族的分子进化研究[博士论文].合肥：安徽农业大学.
Livak K J,Schmittgen T D.2007.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method.Methods,25(5):402-408.
Lynch M,Conery J S.2000.The evolutionary fate and consequences of duplicate genes.Science,290(5494):1151-1155.
McDonald J H,Kreitman M.1991.Adaptive protein evolution at the Adh locus in Drosophila.Nature,352(6328):652-654.
Ooka H,Satoh K,Doi K,Nagata T,Otomo Y,Murakami K,Matsubara K,Osato N,Kawai J,Carninci P,Hayashizaki Y,Suzuki K,Kojima K,Takahara Y,Yamamoto K,Kikuchi S.2003.Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana.DNAResearch,10:239-247.
Qi J J,Liu X,Shen D,Miao H,Xie B Y,Li X X,Zeng P,Wang S H,Shang Y,Gu X F,Du T C,Li Y,Lin T,Yuan J H,Yang X Y,Chen JF,Chen H M,Xiong X Y,Huang K,Fei Z J,Mao L Y,Tian L,Stadler T,Renner S S,Kamoun S,Lucas W J,Zhang Z H,Huang S W.2013.A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity.Nature Genetics,45:12.
Qiao X,Li M,Li L T,Yin H,Wu J Y,Zhang S L.2015.Genome-wide identification and comparative analysis of the heat shock transcription factor family in Chinese white pear(Pyrus bretschneideri)and five other Rosaceae species.BMC Plant Biology,15:12.
Seo P J,Kim M J,Park J Y,Kim S Y,Jeon J,Lee Y H,Kim J,Park C M.2010a.Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis.The Plant Journal,61:661-671.
Seo P J,Kim M J,Song J S,Kim Y S,Kim H J,Park C M.2010b.Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced change in membrane fluidity.Biochemical Society,427:359-367.
Shang Q M,Li L,Dong C J.2012.Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis satives L.Planta,236:1093-1105.
Wang Y P,Tang H B,DeBarry J D,Tan X,Li J P,Wang X Y,Lee T,Jin H Z,Marler B,Guo H,Kissinger J C,Paterson A H.2012.MCScanX:a toolkit for detection and evolutionary analysis of gene synteny and collinearity.Nucleic Acides Research,40(7):e49.
Wang Y P,Wang X Y,Tang H B,Tan X,Ficklin S P,Feltus F A,Paterson A H.2011.Modes of gene duplication contribute differently to genetic novelty and redundancy,but show parallels across divergent angiosperms.PLoS ONE,6(12):e28150.
Waterhouse A,Bertoni M,Bienert S,Studer G,Tauriello G,Gumienny R,Heer F T,Beer T A P,Rempfer C,Bordoli L,Lepore R,Schwede T.2018.SWISS-MODEL:homology modeling of protein structures and complexes.Nucleic Acides Research,1-8.
Wei S W,Gao L G,Zhang Y D,Zhang F R,Yang X,Huang D F.2016.Genome-wide investigation of the NAC transcription factor family in melon(Cucumis melo L.)and their expression analysis under salt stress.Plant Cell Rep,35:1827-1839.
Yang Z.1998.Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution.Mol Biol Evol,15(5):568-73.
Yang Z H.2007.PAML 4:phylogenetic analysis by maximum likelihood.Mol Biol Evol,24(8):1586-1591.
Yang Z,Nielsen R.2002.Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages.Mol Biol Evol,19(6):908-917.
Yu C S,Lin C J,Hwang J K.2004.Predicting subcellular localization of proteins for gram-negative bacteria by support vector machines based on N-peptide composite-ons.Protein Science,13(6):1402-1406.
Zhang X M,Yu H J,Sun C,Deng J,Zhang X,Liu P,Li Y Y,Li Q,Jiang W J.2017.Genome-wide characterization and expression profiling of the NAC genes under abiotic stresses in Cucumis sativus.Plant Physicalogy and Biochemistry,113:98-109.
Zhu M K,Chen G P,Zhang J L,Zhang Y J,Xie Q L,Zhao Z P,Pan Y,Hu Z L.2014.The abiotic stress-responsive NAC-type transcription factor SINAC4 regulates salt and drought tolerance and stress-related genes in tomato(Solanum lycopersicum).Plant Cell Rep,33:1851-1863.
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