花生膜联蛋白基因家族成员的结构和表达分析
|
摘要
植物膜联蛋白(annexin)是一类钙依赖性磷脂结合蛋白,参与调控植物代谢和生长发育并协同调节抗旱、耐盐等多种抗逆反应,其结构在不同植物中具有物种特异性。为系统分析花生膜蛋白基因家族,对30个花生annexin(annexinof Arachis hypogaea, AnnAh)基因进行了生物信息学分析。结果表明30个AnnAhs不均匀分布在13条染色体上,其中A、B基因组中各有13个和17个。AnnAhs含有2～8个内含子,但大多数含有5～6个内含子。聚类分析表明,植物annexin聚类关系比较复杂,低等植物、单子叶、双子叶植物annexin间隔分布, AnnAhs穿插其中,分布于各个分支中;但在各个小分支中,AnnAhs基本上都与双子叶植物annexin聚在一起,其中与大豆、苜蓿、向日葵亲缘关系较近,其次是拟南芥;但个别AnnAhs与单子叶植物和低等植物annexin聚在一起。30个AnnAhs均无跨膜结构域,其中有16个AnnAhs定位于细胞质,其余定位不明确。对AnnAhs可变剪切分析显示,仅有11个发生可变剪切事件,占38%;根中发生的最多,其次是叶中,种子中最少。根据表达谱数据分析发现, AnnAhs在seed2和根中表达量较高,其次是seed1,在叶中表达量较低。本文可为花生抗性育种提供一定的理论支撑。
Annexin is a kind of calcium-dependent phospholipid binding proteins involved in the regulation of plant metabolism,growth and development, drought resistance and salt tolerance, and its structure is species-specific in different plants. In order to have a systematic analysis of the annexin gene family of peanut, we identified 30 annexin genes from the peanut genome database,and analyzed their characteristics using bioinformatics method. Peanut annexin(annexin of Arachis hypogaea, AnnAh) genes were unevenly distributed on 13 chromosomes, with 13 in A genome and 17 in B genome. There were 2 to 8 introns in the AnnAhs, with 5 to 6 introns in most AnnAhs. Phylogenetic analysis showed that the clustering relationship was complex. The annexins of lower plant, monocotyledonous and dicotyledonous plants were distributed at interval, with AnnAhs inserting in each branch. However,in each small branch, AnnAhs were basically clustered with the dicotyledonous plant annexins, and close to soybean, alfalfa and sunflower, followed by Arabidopsis; but several Ann Ahs were associated with monocotyledonous and lower plant annexins. All 30 AnnAhs had no transmembrane domain, and 16 of them were located in cytoplasm, and the others’ localization was uncertain.Results of alternative splicing(AS) analysis of Ann Ahs showed that only 11 AnnAhs experienced AS, which accounted for about 38% of all AnnAhs; the AS events occurred most in roots, followed by leaves, and the least in seeds. The expression level of AnnAhs was high in seed2 and root, followed by seed1, and lower in leaf. The comprehensive analysis of AnnAhs can provide some theoretical support for peanut resistance breeding.
Annexin is a kind of calcium-dependent phospholipid binding proteins involved in the regulation of plant metabolism,growth and development, drought resistance and salt tolerance, and its structure is species-specific in different plants. In order to have a systematic analysis of the annexin gene family of peanut, we identified 30 annexin genes from the peanut genome database,and analyzed their characteristics using bioinformatics method. Peanut annexin(annexin of Arachis hypogaea, AnnAh) genes were unevenly distributed on 13 chromosomes, with 13 in A genome and 17 in B genome. There were 2 to 8 introns in the AnnAhs, with 5 to 6 introns in most AnnAhs. Phylogenetic analysis showed that the clustering relationship was complex. The annexins of lower plant, monocotyledonous and dicotyledonous plants were distributed at interval, with AnnAhs inserting in each branch. However,in each small branch, AnnAhs were basically clustered with the dicotyledonous plant annexins, and close to soybean, alfalfa and sunflower, followed by Arabidopsis; but several Ann Ahs were associated with monocotyledonous and lower plant annexins. All 30 AnnAhs had no transmembrane domain, and 16 of them were located in cytoplasm, and the others’ localization was uncertain.Results of alternative splicing(AS) analysis of Ann Ahs showed that only 11 AnnAhs experienced AS, which accounted for about 38% of all AnnAhs; the AS events occurred most in roots, followed by leaves, and the least in seeds. The expression level of AnnAhs was high in seed2 and root, followed by seed1, and lower in leaf. The comprehensive analysis of AnnAhs can provide some theoretical support for peanut resistance breeding.
引文
[1]Ahmed I,Yadav D,Shukla P,Kirti P B.Heterologous expression of Brassica juncea annexin,AnnBj2 confers salt tolerance and ABA insensitivity in transgenic tobacco seedlings.Funct Integr Genomic,2018,18:569-529.
[2]李瑞梅,王雨晴,张帆,袁帅,耿梦婷,姚远,刘姣,段瑞军,符少萍,胡新文,郭建春.植物膜联蛋白(Annexin)的研究进展.基因组学与应用生物学,2017,36:2128-2136.Li R M,Wang Y Q,Zhang F,Yuan S,Geng M T,Yao Y,Liu J,Duan R G,Fu S P,Hu X W,Guo J C.Research progress on plant annexin.Genomic Appl Biol,2017,36:2128-2136(in Chinese with English abstract).
[3]叶卫华.膜联蛋白A7(annexin A7)在胃癌凋亡中作用的研究.河北医科大学博士学位论文,河北石家庄,2017.Ye W H.The Role of A7(Annexin A7)in Apoptosis of Gastric Carcinoma.PhD Dissertation of Hebei Medical University,Shijiazhuang,Hebei,China,2017(in Chinese with English abstract).
[4]Galv?o I,Vago J P,Barroso L C,Tavares L P,Queiroz-Junior CM,Costa V V,Carneiro F S,Ferreira T P,Silva P M,Amaral F A,Sousa L P,Teixeira M M.Annexin A1 promotes timely resolution of inflammation in murine gout.Eur J Immunol,2017,47:585-596.
[5]Konopkapostupolska D,Clark G.Annexins as overlooked regulators of membrane trafficking in plant cells.Int J Mol Sci,2017,18:863.
[6]Hua K L,Li Y,Zhao Q,Fan L Q,Tan B B,Gu J B.Downregulation of Annexin A11(ANXA11)inhibits cell proliferation,invasion,and migration via the AKT/GSK-3βpathway in gastric cancer.Med Sci Monitor,2018,24:149-160.
[7]Pi F,Zhang H,Li H,Thiviyanathan V,Gorenstein D G,Sood A K,Guo P.RNA nanoparticles harboring annexin A2 aptamer can target ovarian cancer for tumor-specific doxorubicin delivery.Nanomedicine(UK),2017,13:1183-1193.
[8]Yu S,Bian H,Gao X,Gui L.Annexin A9 promotes invasion and metastasis of colorectal cancer and predicts poor prognosis.Int JMol Med,2018,41:2185-2192.
[9]杜锐.Annexin A3(ANXA3)对乳腺癌的调控研究与乳腺癌患者来源移植瘤模型的建立.中国科学技术大学博士学位论文,安徽合肥,2017.Du R.The Role of Annexin A3 in Regulating Breast Cancer and the Establishment of Breast Cancer PDX Model.PhD Dissertation of University of Science and Technology of China,Hefei,Anhui,China,2017(in Chinese with English abstract).
[10]刘琰.Annexin A2对卵巢癌生物学行为的影响及机制研究.郑州大学博士学位论文,河南郑州,2017.Liu Y.The Effects and Mechanism of Annexin A2 on Biological Behavior of Ovarian Cancer.PhD Dissertation of Zhengzhou University,Zhengzhou,Henan,China,2017(in Chinese with English abstract).
[11]Xu L,Tang Y M,Gao S Q,Su S C,Hong L,Wang W W,Fang ZF,Li X Y,Ma J X,Quan W,Sun H,Li X,Wang Y B,Liao X Z,Gao J G,Zhang F G,Li L,Zhao C P.Comprehensive analyses of the annexin gene family in wheat.BMC Genomics,2016,17:415.
[12]Zhang F,Jin X X,Wang L K,Li S F,Wu S,Cheng C Z,Zhang TZ,Guo W Z.A cotton annexin affects fiber elongation and secondary cell wall biosynthesis associated with Ca2+influx,ROShomeostasis,and actin filament reorganization.Plant Physiol,2016,171:1750-1770.
[13]楚璞.莲膜联蛋白的鉴定及其在种子耐热性和活力中的功能研究.中山大学博士学位论文,广东广州,2011.Chu P.Identification and Functional Analysis of a Nelumbo nuciferaa Annexin Involved in Seed Thermotolerance and Vigor.PhD Dissertation of Sun Yat-Sen University.Guangzhou,Guangdong,China,2011(in Chinese with English abstract).
[14]褚翠萍.拟南芥膜联蛋白的基因表达、亚细胞定位和AnnAt3响应非生物胁迫的初步研究.山东农业大学硕士学位论文,山东泰安,2012.Chu C P.Gene Expression,Subcellular Localization of Arabidopsis Annexins and Abiotic Stress Response of Ann At3.MS Thesis of Shandong Agricultural University,Tai’an,Shandong,China,2005(in Chinese with English abstract).
[15]何美敬,穆国俊,侯名语,陈焕英,崔顺立,杨鑫雷,刘立峰.植物膜联蛋白的结构及功能研究进展.西北植物学报,2013,33:2567-2574.He M J,Mu G J,Hou M Y,Chen H Y,Cui S L,Yang X L,Liu L F.Advances in structure and function of plant annexins.Acta Bot Boreali-Occid Sin,2013,33:2567-2574(in Chinese with English abstract).
[16]褚翠萍,任秋萍,孔兰静,王秀玲.拟南芥膜联蛋白2的亚细胞定位研究.中国细胞生物学学报,2017,39:873-880.Zhu C P,Ren Q P,Kong L G,Wang X L.The subcellular localization of annexin 2 in Arabidopsis.Chin J Cell Biol,2017,39:873-880(in Chinese with English abstract).
[17]Clark G B,Dauwalder M,Roux S J.Purification and immunolocalization of an annexin-like protein in pea seedlings.Planta,1992,187:1-9.
[18]Clark G B,Dauwalder M,Roux S J.Immunological and biochemical evidence for nuclear localization of annexin in peas.Plant Physiol Biochem,1998,36:621-627.
[19]Seals D F,Parrish M L,Randall S K.A 42-kilodalton annexin-like protein is associated with plant vacuoles.Plant Physiol,1994,106:1403-1412.
[20]Thonat C,Mathieu C,Crevecoeur M,Penel C,Gaspar T,Boyer N.Effects of a mechanical stimulation of localization of annexin-like proteins in Bryonia dioica internodes.Plant Physiol,1997,114:981-988.
[21]郑昌林.花生基因组中重复基因间基因置换的比较分析.华北理工大学硕士学位论文,河北唐山,2017.Zheng C L.Comparative Analysis of Repetitive Gene Replacement in Peanut Genome.MS Thesis of North China University of Science and Technology,Tangshan,Hebei,China,2017(in Chinese with English abstract).
[22]王靖.花生膜联蛋白基因AnnAh1和AnnAh2的功能验证.山东大学硕士学位论文,山东济南,2014.Wang J.Functional Research of Annexin Gene Ann Ah1 and Ann Ah2 from Arachis hypogaea L.MS Thesis of Shandong University,Jinan,Shandong,China,2017(in Chinese with English abstract).
[23]何美敬,杨鑫雷,崔顺立,穆国俊,侯名语,陈焕英,刘立峰.花生膜联蛋白基因(Annexin)家族的分子克隆和鉴定.中国作物学会学术年会论文集,2014.He M J,Yang X L,Cui S L,Mu G J,Hou M Y,Chen H Y,Liu L F.Molecular cloning and identification of annexin gene family from peanut.In:Proceedings of the Crop Science Society of China,2014(abstract in Chinese).
[24]Trapnell C,Williams B A,Pertea G,Mortazavi A,Kwan G,van Baren M J,Salzberg S L,Wold B J.Transcript assembly and quantification by RNA Seq reveals unannotated transcripts and isoform switching during cell differentiation.Nat Biotechnol,2010,28:511-515.
[25]Florea L,Li S,Salzberg S L.Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues.Eur PMC,2013,2:188.
[26]Clark G B,Dauwalder M,Roux S J.Immunolocalization of an annexin-like protein in corn.Adv Space Res,1994,14:341-346.
[27]Jami S K,Clark G B,Ayele B T,Ashe P,Kirti P B.Genome-wide comparative analysis of annexin superfamily in plants.PLoS One,2012,7:47801.
[28]王立科,张边江,唐宁,杨平,周峰,陈全战.植物膜联蛋白基因研究进展.分子植物育种,2016,14:2060-2065.Wang L K,Zhang B J,Tang N,Yang P,Zhou F,Chen Q Z.Research advances of annexin genes in plants.Mol Plant Breed,2016,14:2060-2065(in Chinese with English abstract).
[29]Vogel C,Chothia C.Protein family expansions and biological complexity.PLoS Comput Biol,2006,2:48.
[30]Schmutz J,Cannon S B,Schlueter J,Ma J X,Mitros T,Nelson W,Hyten D L,Song Q J,Thelen J J,Cheng J L,Xu D,Hellsten U,May G D,Yu Y,Sakurai T,Umezawa T,Bhattacharyya M K,Sandhu D,Valliyodan B,Lindquist E,Peto M,Grant D,Shu S Q,Goodstein D,Barry K,Futrell-Griggs M,Abernathy B,Du J C,Tian Z X,Zhu L C,Gill N,Joshi T,Libault M,Sethuraman A,Zhang X C,Shinozaki K,Nguyen H T,Wing R A,Cregan P,Specht J,Grimwood J,Rokhsar D,Stacey G,Shoemaker R C,Jackson S A.Genome sequence of the palaeopolyploid soybean.Nature,2010,463:178-183.
[31]Kandasamy M K,Burgos-Rivera B,McKinney E C,Ruzicka D R,Meagher R B.Class-specific interaction of profilin and ADFisovariants with actin in the regulation of plant development.Plant Cell,2007,19:3111-3126.
[32]Koehler P E,Odell G V.Factors affecting the formation of pyrazine compounds in sugara-mine reactions.J Agric Food Chem,1970,18:895-898.
[33]Clark G B,Sessions A,Eastburn D J,Roux S J.Differential expression of members of the annexin multigene family in Arabidopsis.Plant Physiol,2001,126:1072-1084.
[34]李立奇,万瑛.蛋白质的亚细胞定位预测研究进展.免疫学杂志,2009,25:602-604.Li L Q,Wan Y.Advancement of predicting proteins in subcellular localization sites.Immunol J,2009,25:602-604(in Chinese with English abstract).
[35]李兵.棉花(Gossypium hirsutum)膜联蛋白基因克隆鉴定及功能研究.华中师范大学博士学位论文,湖北武汉,2012.Li B.Molecular Characterization and Function of the Cotton Annexin Genes.PhD Dissertation of Central China normal University,Wuhan,Hubei,China,2012(in Chinese with English abstract).
[36]王雨晴,张帆,李瑞梅,胡新文,郭建春.木薯MeAnn1基因的克隆及表达分析.分子植物育种,2015,13:2477-2483.Wang Y Q,Zhang F,Li R M,Hu X W,Guo J C.Cloning and expression of MeAnn1 gene from cassava(Manihot esculenta Crantz).Mol plant breed,2015,13:2477-2483(in Chinese with English abstract).
[37]Breton G,Vazqueztello A,Danyluk J,Sarhan F.Two novel intrinsic annexins accumulate in wheat membranes in response to low temperature.Plant Cell Physiol,2000,41:177-184.
[38]Carvalho-Niebel F D,Timmers A C J,Chabaud M,Defaux-Petras A,Barker D G.The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula.Plant J,2002,32:343-352.
[39]章天骄.可变剪接的生物信息数据分析综述.生物信息学,2012,10:61-64.Zhang T J.Review of bioinformation data analysis with alternative splicing.Chin J Bioinformatic,2012,10:61-64(in Chinese with English abstract).
[40]Wilkinson J Q,Lanahan M B,Conner T W,Klee H J.Identification of mRNAs with enhanced expression in ripening strawberry fruit using polymerase chain reaction differential display.Plant Mol Biol,1995,27:1097-1108.
[41]那杰,杨怀义.植物Annexins研究进展.辽宁师范大学学报(自然科学版),2004,27:464-467.Na J,Yang H Y.Aadvances in the study of plant annexins.JLiaoning Norm Univ(Nat Sci Edn),2004,27:464-467(in Chinese with English abstract)
[42]Baucher M,Oukouomi L Y,Vandeputte O M,Bopopi J M,Moussawi J,Vermeersch M,Mol A,Jaziri M E,Homble F,Perez-Morga D.Ntann12 annexin expression is induced by auxin in tobacco roots.J Exp Bot,2011,62:4055-4065.
[43]巩子英,宋雪,陈功友,朱家璧,俞冠翘,邹华松.苜蓿膜联蛋白MtAnn3基因的鉴定及其在根毛发育中的功能.科学通报,2012,57:431-437.Gong Z Y,Song X,Chen G Y,Zhu J B,Yu G Q,Zou H S.Identification of MtAnn3 gene of alfalfa and its function in root hair development.Chin Sci Bull,2012,57:431-437(in Chinese).
[2]李瑞梅,王雨晴,张帆,袁帅,耿梦婷,姚远,刘姣,段瑞军,符少萍,胡新文,郭建春.植物膜联蛋白(Annexin)的研究进展.基因组学与应用生物学,2017,36:2128-2136.Li R M,Wang Y Q,Zhang F,Yuan S,Geng M T,Yao Y,Liu J,Duan R G,Fu S P,Hu X W,Guo J C.Research progress on plant annexin.Genomic Appl Biol,2017,36:2128-2136(in Chinese with English abstract).
[3]叶卫华.膜联蛋白A7(annexin A7)在胃癌凋亡中作用的研究.河北医科大学博士学位论文,河北石家庄,2017.Ye W H.The Role of A7(Annexin A7)in Apoptosis of Gastric Carcinoma.PhD Dissertation of Hebei Medical University,Shijiazhuang,Hebei,China,2017(in Chinese with English abstract).
[4]Galv?o I,Vago J P,Barroso L C,Tavares L P,Queiroz-Junior CM,Costa V V,Carneiro F S,Ferreira T P,Silva P M,Amaral F A,Sousa L P,Teixeira M M.Annexin A1 promotes timely resolution of inflammation in murine gout.Eur J Immunol,2017,47:585-596.
[5]Konopkapostupolska D,Clark G.Annexins as overlooked regulators of membrane trafficking in plant cells.Int J Mol Sci,2017,18:863.
[6]Hua K L,Li Y,Zhao Q,Fan L Q,Tan B B,Gu J B.Downregulation of Annexin A11(ANXA11)inhibits cell proliferation,invasion,and migration via the AKT/GSK-3βpathway in gastric cancer.Med Sci Monitor,2018,24:149-160.
[7]Pi F,Zhang H,Li H,Thiviyanathan V,Gorenstein D G,Sood A K,Guo P.RNA nanoparticles harboring annexin A2 aptamer can target ovarian cancer for tumor-specific doxorubicin delivery.Nanomedicine(UK),2017,13:1183-1193.
[8]Yu S,Bian H,Gao X,Gui L.Annexin A9 promotes invasion and metastasis of colorectal cancer and predicts poor prognosis.Int JMol Med,2018,41:2185-2192.
[9]杜锐.Annexin A3(ANXA3)对乳腺癌的调控研究与乳腺癌患者来源移植瘤模型的建立.中国科学技术大学博士学位论文,安徽合肥,2017.Du R.The Role of Annexin A3 in Regulating Breast Cancer and the Establishment of Breast Cancer PDX Model.PhD Dissertation of University of Science and Technology of China,Hefei,Anhui,China,2017(in Chinese with English abstract).
[10]刘琰.Annexin A2对卵巢癌生物学行为的影响及机制研究.郑州大学博士学位论文,河南郑州,2017.Liu Y.The Effects and Mechanism of Annexin A2 on Biological Behavior of Ovarian Cancer.PhD Dissertation of Zhengzhou University,Zhengzhou,Henan,China,2017(in Chinese with English abstract).
[11]Xu L,Tang Y M,Gao S Q,Su S C,Hong L,Wang W W,Fang ZF,Li X Y,Ma J X,Quan W,Sun H,Li X,Wang Y B,Liao X Z,Gao J G,Zhang F G,Li L,Zhao C P.Comprehensive analyses of the annexin gene family in wheat.BMC Genomics,2016,17:415.
[12]Zhang F,Jin X X,Wang L K,Li S F,Wu S,Cheng C Z,Zhang TZ,Guo W Z.A cotton annexin affects fiber elongation and secondary cell wall biosynthesis associated with Ca2+influx,ROShomeostasis,and actin filament reorganization.Plant Physiol,2016,171:1750-1770.
[13]楚璞.莲膜联蛋白的鉴定及其在种子耐热性和活力中的功能研究.中山大学博士学位论文,广东广州,2011.Chu P.Identification and Functional Analysis of a Nelumbo nuciferaa Annexin Involved in Seed Thermotolerance and Vigor.PhD Dissertation of Sun Yat-Sen University.Guangzhou,Guangdong,China,2011(in Chinese with English abstract).
[14]褚翠萍.拟南芥膜联蛋白的基因表达、亚细胞定位和AnnAt3响应非生物胁迫的初步研究.山东农业大学硕士学位论文,山东泰安,2012.Chu C P.Gene Expression,Subcellular Localization of Arabidopsis Annexins and Abiotic Stress Response of Ann At3.MS Thesis of Shandong Agricultural University,Tai’an,Shandong,China,2005(in Chinese with English abstract).
[15]何美敬,穆国俊,侯名语,陈焕英,崔顺立,杨鑫雷,刘立峰.植物膜联蛋白的结构及功能研究进展.西北植物学报,2013,33:2567-2574.He M J,Mu G J,Hou M Y,Chen H Y,Cui S L,Yang X L,Liu L F.Advances in structure and function of plant annexins.Acta Bot Boreali-Occid Sin,2013,33:2567-2574(in Chinese with English abstract).
[16]褚翠萍,任秋萍,孔兰静,王秀玲.拟南芥膜联蛋白2的亚细胞定位研究.中国细胞生物学学报,2017,39:873-880.Zhu C P,Ren Q P,Kong L G,Wang X L.The subcellular localization of annexin 2 in Arabidopsis.Chin J Cell Biol,2017,39:873-880(in Chinese with English abstract).
[17]Clark G B,Dauwalder M,Roux S J.Purification and immunolocalization of an annexin-like protein in pea seedlings.Planta,1992,187:1-9.
[18]Clark G B,Dauwalder M,Roux S J.Immunological and biochemical evidence for nuclear localization of annexin in peas.Plant Physiol Biochem,1998,36:621-627.
[19]Seals D F,Parrish M L,Randall S K.A 42-kilodalton annexin-like protein is associated with plant vacuoles.Plant Physiol,1994,106:1403-1412.
[20]Thonat C,Mathieu C,Crevecoeur M,Penel C,Gaspar T,Boyer N.Effects of a mechanical stimulation of localization of annexin-like proteins in Bryonia dioica internodes.Plant Physiol,1997,114:981-988.
[21]郑昌林.花生基因组中重复基因间基因置换的比较分析.华北理工大学硕士学位论文,河北唐山,2017.Zheng C L.Comparative Analysis of Repetitive Gene Replacement in Peanut Genome.MS Thesis of North China University of Science and Technology,Tangshan,Hebei,China,2017(in Chinese with English abstract).
[22]王靖.花生膜联蛋白基因AnnAh1和AnnAh2的功能验证.山东大学硕士学位论文,山东济南,2014.Wang J.Functional Research of Annexin Gene Ann Ah1 and Ann Ah2 from Arachis hypogaea L.MS Thesis of Shandong University,Jinan,Shandong,China,2017(in Chinese with English abstract).
[23]何美敬,杨鑫雷,崔顺立,穆国俊,侯名语,陈焕英,刘立峰.花生膜联蛋白基因(Annexin)家族的分子克隆和鉴定.中国作物学会学术年会论文集,2014.He M J,Yang X L,Cui S L,Mu G J,Hou M Y,Chen H Y,Liu L F.Molecular cloning and identification of annexin gene family from peanut.In:Proceedings of the Crop Science Society of China,2014(abstract in Chinese).
[24]Trapnell C,Williams B A,Pertea G,Mortazavi A,Kwan G,van Baren M J,Salzberg S L,Wold B J.Transcript assembly and quantification by RNA Seq reveals unannotated transcripts and isoform switching during cell differentiation.Nat Biotechnol,2010,28:511-515.
[25]Florea L,Li S,Salzberg S L.Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues.Eur PMC,2013,2:188.
[26]Clark G B,Dauwalder M,Roux S J.Immunolocalization of an annexin-like protein in corn.Adv Space Res,1994,14:341-346.
[27]Jami S K,Clark G B,Ayele B T,Ashe P,Kirti P B.Genome-wide comparative analysis of annexin superfamily in plants.PLoS One,2012,7:47801.
[28]王立科,张边江,唐宁,杨平,周峰,陈全战.植物膜联蛋白基因研究进展.分子植物育种,2016,14:2060-2065.Wang L K,Zhang B J,Tang N,Yang P,Zhou F,Chen Q Z.Research advances of annexin genes in plants.Mol Plant Breed,2016,14:2060-2065(in Chinese with English abstract).
[29]Vogel C,Chothia C.Protein family expansions and biological complexity.PLoS Comput Biol,2006,2:48.
[30]Schmutz J,Cannon S B,Schlueter J,Ma J X,Mitros T,Nelson W,Hyten D L,Song Q J,Thelen J J,Cheng J L,Xu D,Hellsten U,May G D,Yu Y,Sakurai T,Umezawa T,Bhattacharyya M K,Sandhu D,Valliyodan B,Lindquist E,Peto M,Grant D,Shu S Q,Goodstein D,Barry K,Futrell-Griggs M,Abernathy B,Du J C,Tian Z X,Zhu L C,Gill N,Joshi T,Libault M,Sethuraman A,Zhang X C,Shinozaki K,Nguyen H T,Wing R A,Cregan P,Specht J,Grimwood J,Rokhsar D,Stacey G,Shoemaker R C,Jackson S A.Genome sequence of the palaeopolyploid soybean.Nature,2010,463:178-183.
[31]Kandasamy M K,Burgos-Rivera B,McKinney E C,Ruzicka D R,Meagher R B.Class-specific interaction of profilin and ADFisovariants with actin in the regulation of plant development.Plant Cell,2007,19:3111-3126.
[32]Koehler P E,Odell G V.Factors affecting the formation of pyrazine compounds in sugara-mine reactions.J Agric Food Chem,1970,18:895-898.
[33]Clark G B,Sessions A,Eastburn D J,Roux S J.Differential expression of members of the annexin multigene family in Arabidopsis.Plant Physiol,2001,126:1072-1084.
[34]李立奇,万瑛.蛋白质的亚细胞定位预测研究进展.免疫学杂志,2009,25:602-604.Li L Q,Wan Y.Advancement of predicting proteins in subcellular localization sites.Immunol J,2009,25:602-604(in Chinese with English abstract).
[35]李兵.棉花(Gossypium hirsutum)膜联蛋白基因克隆鉴定及功能研究.华中师范大学博士学位论文,湖北武汉,2012.Li B.Molecular Characterization and Function of the Cotton Annexin Genes.PhD Dissertation of Central China normal University,Wuhan,Hubei,China,2012(in Chinese with English abstract).
[36]王雨晴,张帆,李瑞梅,胡新文,郭建春.木薯MeAnn1基因的克隆及表达分析.分子植物育种,2015,13:2477-2483.Wang Y Q,Zhang F,Li R M,Hu X W,Guo J C.Cloning and expression of MeAnn1 gene from cassava(Manihot esculenta Crantz).Mol plant breed,2015,13:2477-2483(in Chinese with English abstract).
[37]Breton G,Vazqueztello A,Danyluk J,Sarhan F.Two novel intrinsic annexins accumulate in wheat membranes in response to low temperature.Plant Cell Physiol,2000,41:177-184.
[38]Carvalho-Niebel F D,Timmers A C J,Chabaud M,Defaux-Petras A,Barker D G.The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula.Plant J,2002,32:343-352.
[39]章天骄.可变剪接的生物信息数据分析综述.生物信息学,2012,10:61-64.Zhang T J.Review of bioinformation data analysis with alternative splicing.Chin J Bioinformatic,2012,10:61-64(in Chinese with English abstract).
[40]Wilkinson J Q,Lanahan M B,Conner T W,Klee H J.Identification of mRNAs with enhanced expression in ripening strawberry fruit using polymerase chain reaction differential display.Plant Mol Biol,1995,27:1097-1108.
[41]那杰,杨怀义.植物Annexins研究进展.辽宁师范大学学报(自然科学版),2004,27:464-467.Na J,Yang H Y.Aadvances in the study of plant annexins.JLiaoning Norm Univ(Nat Sci Edn),2004,27:464-467(in Chinese with English abstract)
[42]Baucher M,Oukouomi L Y,Vandeputte O M,Bopopi J M,Moussawi J,Vermeersch M,Mol A,Jaziri M E,Homble F,Perez-Morga D.Ntann12 annexin expression is induced by auxin in tobacco roots.J Exp Bot,2011,62:4055-4065.
[43]巩子英,宋雪,陈功友,朱家璧,俞冠翘,邹华松.苜蓿膜联蛋白MtAnn3基因的鉴定及其在根毛发育中的功能.科学通报,2012,57:431-437.Gong Z Y,Song X,Chen G Y,Zhu J B,Yu G Q,Zou H S.Identification of MtAnn3 gene of alfalfa and its function in root hair development.Chin Sci Bull,2012,57:431-437(in Chinese).