柑橘U-box基因家族的鉴定及表达分析
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摘要
【目的】通过生物信息学分析U-box在柑橘基因组中的分布、结构及进化,研究家族成员在不同组织中的表达特异性以及对非生物胁迫和激素的响应,解析柑橘U-box基因家族的生物学功能。【方法】根据已经报道的拟南芥U-box基因,利用Phytozome数据库中的BLASTp工具鉴定柑橘基因组中的U-box基因。采用MEGA6.0、Cello、SMART、GSDS2.0、ExPASy和MapChart等软件构建系统进化树、亚细胞定位预测、预测蛋白的相对分子质量与等电点等理化性质、绘制家族成员Scaffold定位图等,分析U-box基因家族在低温胁迫下表达模式,利用实时荧光定量PCR技术(q RT-PCR)检测柑橘U-box基因家族部分成员在NaCl、PEG6000和不同激素处理下的表达情况。【结果】从柑橘克里曼丁(Citrus clementina)全基因组中鉴定出56个Cc PUBs基因家族成员,可将其分为7类,即U-box only、U-box+ARM-1、U-box+WD40-1、TPR+U-box、Kinase+U-box、U-box+ARM-2和U-box+WD40-2。该家族蛋白理论等电点分布在5.19—9.14,编码的氨基酸数目介于281—1 441;亚细胞定位预测结果显示该基因家族成员位于细胞不同位置,主要位于细胞核或叶绿体,少数位于质膜;聚类分析发现,柑橘U-box与单子叶植物水稻的亲缘关系较远,柑橘中具有相同结构域的成员和拟南芥具有相同结构域的成员聚在一起,表明柑橘U-box成员具有不同生物学功能;Scaffold定位分析发现,56个U-box成员分布在1—9 Scafflod上且呈不均分布。在冷胁迫下的RNA-Seq分析结果表明,U-box基因家族参与植物对冷胁迫的应答,并表现出4种不同的应答模式;从柑橘U-box基因家族的5个不同簇上分别选取1个代表基因进行qRT-PCR,分析结果表明,Cc PUB48在金柑的各个组织中均有表达,CcPUB9和CcPUB4主要在茎和花中表达,Cc PUB10主要在花、茎和幼果中表达,CcPUB41主要在叶和茎中表达,体现了不同U-box成员的组织特异性的表达差异。CcPUB4、CcPUB10和CcPUB41在Na Cl胁迫下表达均上调,而CcPUB48在盐胁迫下的表达无明显变化。Cc PUB4在Na2CO3处理下表达明显上调,与Na Cl处理存在一致的表达趋势,而Ca Cl2处理下的表达与Na Cl处理下的表达趋势却存在差异。在PEG6000的处理条件下,CcPUB4的表达量呈现先上升后下降的趋势,CcPUB9、CcPUB41和Cc PUB48在PEG6000的处理下无明显变化。在赤霉素(GA3)处理下,Cc PUB4在3 h时明显上调,在生长素(IAA)和脱落酸(ABA)下呈现无规律变化,CcPUB10在ABA处理下表达量表现出逐渐上升。【结论】从柑橘克里曼丁全基因组上鉴定出56个U-box基因成员,各成员均含有U-box保守结构域,并位于细胞的不同位置。U-box基因家族参与植物对冷胁迫的应答并表现出4种不同的应答模式,在Na Cl、PEG6000和激素处理下,Cc PUB4和Cc PUB10有不同程度的响应,而Cc PUB9、CcPUB41和Cc PUB48响应不明显或未响应。
【Objective】 The objectives of this study were to analyze the distribution, structure and evolution of U-box in citrus genome by bioinformatics, to study the expression specificity of family members in different tissues and their responses to abiotic stress and hormones, and to investigate the biological function of U-box gene family in citrus. 【Method】 According to the reported U-box gene of Arabidopsis thaliana, the U-box gene in citrus genome was identified by BLASTp tool in Phytozome database.Phylogenetic tree, subcellular localization prediction, relative mass and isoelectric point and other physical and chemical properties,and scaffold location of U-box member were analyzed with MEGA6.0, Cello, SMART, GSDS2.0, ExPASy and MapChart,respectively. The expression pattern of U-box gene family under low temperature stress was analyzed, and the expression of some members of U-box gene family in citrus treated with NaCl, PEG6000 and different hormones was detected by real-time fluorescence quantitative PCR(qRT-PCR).【Result】Fifty-six members of CcPUBs gene family were identified from the whole genome of Citrus clementina, and they could be divided into 7 categories, namely as U-box only, U-box+ARM-1, U-box+WD40-1, TPR+U-box,Kinase+U-box, U-box+ARM-2 and U-box+WD40-2. The theoretical isoelectric point of the family protein was ranged from 5.19 to9.14, and the number of amino acids encoded was 281 to 1 441. The results of subcellular localization prediction showed that the members of the gene family were located in different positions of the cell, mainly in the nucleus or chloroplast, and a few in the plasma membrane. Cluster analysis showed that citrus U-box was closely related to monocotyledonous rice, and members with the same domain in citrus and Arabidopsis thaliana were clustered together. The results showed that U-box members of citrus had different biological functions, and scaffold localization analysis showed that 56 U-box members were unevenly distributed on citrus1-9 scaffold. The results of RNA-Seq analysis under cold stress showed that U-box gene family was involved in the response of plants to cold stress and showed four different response patterns. One representative gene was selected respectively from five different clusters of citrus U-box gene family for qRT-PCR analysis. The results showed that CcPUB48 was expressed in all tissues of kumquat, and CcPUB9 and CcPUB4 were mainly expressed in stems and flowers, CcPUB10 was mainly expressed in flowers,stems and young fruits, and Cc PUB41 was mainly expressed in leaves and stems. It reflected the tissue-specific expression difference of different U-box members. The expression of CcPUB4, CcPUB10 and CcPUB41 was up-regulated under NaCl stress,but the expression of CcPUB48 had no significant change under salt stress. The expression of CcPUB4 was up-regulated under Na2 CO3 treatment, which was consistent with that of NaCl treatment, but the expression trend of CaCl2 treatment was different from that of NaCl treatment. Under the treatment of PEG6000, the expression of CcPUB4 increased at first and then decreased,while CcPUB9, CcPUB41 and CcPUB48 did not change significantly under the treatment of PEG6000. Under gibberellin(GA3)treatment, CcPUB4 was significantly up-regulated at 3 h, while under auxin(IAA) and abscisic acid(ABA), the expression of CcPUB10 showed irregular changes, and the expression of CcPUB10 increased gradually under gibberellin(gibberellin) treatment.【 Conclusion 】 Fifty-six members of U-box gene were identified from the whole genome of Citrus clementina. All members contained U-box conserved domain and were located in different positions of cells. U-box gene family was involved in the response of plants to cold stress and showed four different response patterns. Under NaCl, PEG6000 and hormone treatment, CcPUB4 and CcPUB10 had different degrees of response, but CcPUB9, Cc PUB41 and CcPUB48 had no obvious or no response. This experiment provided a theoretical guidance for the further study of U-box gene family in citrus stress resistance and growth and development mechanism.
【Objective】 The objectives of this study were to analyze the distribution, structure and evolution of U-box in citrus genome by bioinformatics, to study the expression specificity of family members in different tissues and their responses to abiotic stress and hormones, and to investigate the biological function of U-box gene family in citrus. 【Method】 According to the reported U-box gene of Arabidopsis thaliana, the U-box gene in citrus genome was identified by BLASTp tool in Phytozome database.Phylogenetic tree, subcellular localization prediction, relative mass and isoelectric point and other physical and chemical properties,and scaffold location of U-box member were analyzed with MEGA6.0, Cello, SMART, GSDS2.0, ExPASy and MapChart,respectively. The expression pattern of U-box gene family under low temperature stress was analyzed, and the expression of some members of U-box gene family in citrus treated with NaCl, PEG6000 and different hormones was detected by real-time fluorescence quantitative PCR(qRT-PCR).【Result】Fifty-six members of CcPUBs gene family were identified from the whole genome of Citrus clementina, and they could be divided into 7 categories, namely as U-box only, U-box+ARM-1, U-box+WD40-1, TPR+U-box,Kinase+U-box, U-box+ARM-2 and U-box+WD40-2. The theoretical isoelectric point of the family protein was ranged from 5.19 to9.14, and the number of amino acids encoded was 281 to 1 441. The results of subcellular localization prediction showed that the members of the gene family were located in different positions of the cell, mainly in the nucleus or chloroplast, and a few in the plasma membrane. Cluster analysis showed that citrus U-box was closely related to monocotyledonous rice, and members with the same domain in citrus and Arabidopsis thaliana were clustered together. The results showed that U-box members of citrus had different biological functions, and scaffold localization analysis showed that 56 U-box members were unevenly distributed on citrus1-9 scaffold. The results of RNA-Seq analysis under cold stress showed that U-box gene family was involved in the response of plants to cold stress and showed four different response patterns. One representative gene was selected respectively from five different clusters of citrus U-box gene family for qRT-PCR analysis. The results showed that CcPUB48 was expressed in all tissues of kumquat, and CcPUB9 and CcPUB4 were mainly expressed in stems and flowers, CcPUB10 was mainly expressed in flowers,stems and young fruits, and Cc PUB41 was mainly expressed in leaves and stems. It reflected the tissue-specific expression difference of different U-box members. The expression of CcPUB4, CcPUB10 and CcPUB41 was up-regulated under NaCl stress,but the expression of CcPUB48 had no significant change under salt stress. The expression of CcPUB4 was up-regulated under Na2 CO3 treatment, which was consistent with that of NaCl treatment, but the expression trend of CaCl2 treatment was different from that of NaCl treatment. Under the treatment of PEG6000, the expression of CcPUB4 increased at first and then decreased,while CcPUB9, CcPUB41 and CcPUB48 did not change significantly under the treatment of PEG6000. Under gibberellin(GA3)treatment, CcPUB4 was significantly up-regulated at 3 h, while under auxin(IAA) and abscisic acid(ABA), the expression of CcPUB10 showed irregular changes, and the expression of CcPUB10 increased gradually under gibberellin(gibberellin) treatment.【 Conclusion 】 Fifty-six members of U-box gene were identified from the whole genome of Citrus clementina. All members contained U-box conserved domain and were located in different positions of cells. U-box gene family was involved in the response of plants to cold stress and showed four different response patterns. Under NaCl, PEG6000 and hormone treatment, CcPUB4 and CcPUB10 had different degrees of response, but CcPUB9, Cc PUB41 and CcPUB48 had no obvious or no response. This experiment provided a theoretical guidance for the further study of U-box gene family in citrus stress resistance and growth and development mechanism.
引文
[1]SMALLE J,VIERSTRA R D.The ubiquitin 26S proteasome proteolytic pathway.Annual Review of Plant Biology,2004,55:555-590.
[2]刘锴栋,袁长春.泛素/26S蛋白酶体途径及其在植物生长发育中的功能.基因组学与应用生物学,2009,28(6):1219-1228.LIU Y D,YUAN C C.The ubiquitin/26S proteasome pathway and the function in plant development.Genomics and Applied Biology,2009,28(6):1219-1228.(in Chinese)
[3]宋素胜,谢道昕.泛素蛋白酶体途径及其对植物生长发育的调控.植物学通报,2006,23(5):564-577.SONG S S,XIE D X.The ubiquitin-proteosome pathway and plant development.Bulletin of Botany,2006,23(5):564-577.(in Chinese)
[4]VANDEMARK A P,HILL C P.Structural basis of ubiquitylation.Current Opinion Structural Biology,2002,12(6):822-830.
[5]HATAKEYAMA S,YADA M,MATSUMOTO M,ISHIDA N,NAKAYAMA K I.U-box proteins as a new family of ubiquitinprotein ligases.The Journal of Biological Chemistry,2001,276(35):33111-33120.
[6]PATTERSON C.A new gun in town:the U-box is a ubiquitin ligase domain.Science’s STKE,2002,2002(116):pe4.
[7]FARMER L M,BOOK A J,LEE K H,LIN Y L,FU H,VIERSTRA RD.The RAD23 family provides an essential connection between the26S proteasome and ubiquitylated proteins in Arabidopsis.The Plant Cell,2010,22(1):124-142.
[8]VIERSTRA R D.The ubiquitin-26S proteasome system at the nexus of plant biology.Nature Reviews Molecular Cell Biology,2009,10(6):385-397.
[9]GONZALEZ-LAMOTHE R,TSITSIGIANNIS D I,LUDWIG A A,PANICOT M,SHIRASU K,JONES J D G.The U-Box protein CMPG1is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato.Plant Cell,2006,18(4):1067-1083.
[10]CHO S K,CHUNG H S,RYU M Y,PARK M J,LEE M M,BAHK Y,KIM J,PAI H S,KIM W T.Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-box E3 ubiquitin ligases homolog.Plant Physiology,2006,142(4):1664-1682.
[11]LIU Y C,WU Y R,HUANG X H,SUN J,XIE Q.At PUB19,a U-Box E3 ubiquitin ligase,negatively regulates abscisic acid and drought responses in Arabidopsis thaliana.Molecular Plant,2011,4(6):938-946.
[12]HWANG J H,SEO D H,KANG B G,KWAK J M,KIM W T.Suppression of Arabidopsis AtPUB30 resulted in increased tolerance to salt stress during germination.Plant Cell Reports,2015,34(2):277-289.
[13]BRAUMANN I,URBAN W,PREUβA,DOCKTER C,ZAKHRABEKOVA S,HANSSON M.Semi-dwarf barley(Hordeum vulgare L.)brh2 and ari-l mutants are deficient in a U-box E3ubiquitin ligase.Plant Growth Regulation,2018,86(2):223-234.
[14]SAMUEL M A,MUDGIL Y,SALT J N,DELMAS F,RAMACHANDRAN S,CHILELLI A,GORING D R.Interactions between the S-Domain receptor kinases and At PUB-ARM E3ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis.Plant Physiology,2008,147(4):2084-2095.
[15]WU G,TEROL J,IBANEZ V,LOPEZ-GARCIA A,PEREZ-ROMANE,BORREDA C,DOMINGO C,TADEO F R,CARBONELL-CABALLERO J,ALONSO R,CURK F,DU D,OLLITRAULT P,ROOSE M L,DOPAZO J,GMITTER F G,ROKHSAR D S,TALONM.Genomics of the origin and evolution of Citrus.Nature,2018,554(7692):311-316.
[16]郑兴卫,邵麟惠,李聪.蒺藜苜蓿全基因组中U-box基因家族的筛选与特征分析.草业学报,2015,24(8):130-141.ZHENG X W,SHAO L H,LI C.Genome-wide screening and characterization of the U-box gene family in Medicago truncatula.Acta Prataculturase Sinica,2015,24(8):130-141.(in Chinese)
[17]WIBORG J,O'SHEA C,SKRIVER K.Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin-protein ligases.Biochemical Journal,2008,413(3):447-457.
[18]曹英豪.水稻U-box基因家族的特征及转录表达模式分析[D].保定:河北农业大学,2010.CAO Y H.The characteristics of Rice U-Box gene family with its transcription and expression pattern analysis[D].Baoding:Agricultural University of Hebei,2010.(in Chinese)
[19]李菲,何小红,龚记熠.番茄基因组中U-box基因家族的鉴定与分析.分子植物育种.2018,16(11):3468-3476LI F,HE X H,GONG J Y.Identification and analysis of U-box gene family in tomato genome.Molecular Plant Breeding,2018,16(11):3468-3476.(in Chinese)
[20]刘永昌,曾丽亚,盘俊,齐成媚,袁志辉,何福林,胡克坚,刘小文.雷蒙德氏棉Plant U-box(GrPUBs)基因家族生物信息学分析.分子植物育种,2018,16(13):4157-4171.LIU Y C,ZENG L Y,PAN J,QI C M,YUAN Z H,HE F L,HU K J,LIU X W.Bioinformatics analysis of the plant U-box gene families(Gr PUBs)in Gossypium raimondii.Molecular Plant Breeding,2018,16(13):4157-4171.(in Chinese)
[21]IGNACIO M.Ancient origin of animal U-box ubiquitin ligases.BMCEvolutionary Biology,2010,10(1):331.
[22]CONSORTIUM T T G.The tomato genome sequence provides insights into fleshy fruit evolution.Nature,2012,485(7400):635.
[23]LUO J,SHEN G,YAN J,HE C,ZHANG H.At CHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment.The Plant Journal,2006,46(4):649-657.
[24]ADLER G,KONRAD Z,ZAMIR L,MISHRA A K,RAVEH D,BAR-ZVI D.The Arabidopsis paralogs,PUB46 and PUB48,encoding U-box E3 ubiquitin ligases,are essential for plant response to drought stress.BMC Plant Biology,2017,17(1):8.
[25]BERGLER J,HOTH S.Plant U-box armadillo repeat proteins At PUB18 and At PUB19 are involved in salt inhibition of germination in Arabidopsis.Plant Biology,2011,13(5):725-730.
[26]SADANANDOM A.The U-box protein At PUB17 is a functional ortholog of NtACRE276 and its E3 ubiquitin ligase activity is required for plant cell death and defence.Comparative Biochemistry&Physiology Part A,2007,146(4):S203-S203.
[27]SANKARANARAYANAN S,SAMUEL M A.A proposed role for selective autophagy in regulating auxin-dependent lateral root development under phosphate starvation in Arabidopsis.Plant Signaling&Behavior,2015,10(3):e989749.
[28]齐晨辉,赵先炎,韩朋良.苹果U-box型E3泛素连接酶MdPUB24的耐盐性和ABA敏感性鉴定.园艺学报,2017,44(12):2255-2264.QI C H,ZHAO X Y,HAN P L.Functional identification of salt tolerance and ABA sensitivity of apple U-box E3 ubiquitin ligase MdPUB24.Acta Horticulturae Sinica,2017,44(12):2255-2264.(in Chinese)
[29]LIU J,LI W,NING Y,SHIRSEKAR G,CAI Y,WANG X,DAI L,WANG Z,LIU W,WANG G L.The U-Box E3 ligase SPL11/PUB13is a convergence point of defense and flowering signaling in plants.Plant Physiology,2012,160(1):28-37.
[30]SHARMA M,PANDEY G K.Expansion and function of repeat domain proteins during stress and development in plants.Frontiers in Plant Science,2016,6:1218.
[31]SANTNER A,CALDERON-VILLALOBOS L I A,ESTELLE M.Plant hormones are versatile chemical regulators of plant growth.Nature Chemical Biology,2009,5(5):301-307.
[32]HWANG J H,DONG H S,KANG B G,KWAK J M,KIM W T.Suppression of Arabidopsis,At PUB30,resulted in increased tolerance to salt stress during germination.Plant Cell Reports,2015,34(2):277-289.
[33]CHO S K,CHUANG H S,RYU M Y,PARK M J,LEE M M,BAHKY,KIM J,PAI H S,KIM W T.Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog.Plant Physiology,2006,142(4):1664-1682.
[34]KOBAYASHI S,TSUGAMA D,LIU S,TAKANO T.A U-Box E3ubiquitin ligase,PUB20,interacts with the Arabidopsis G-Proteinβsubunit,AGB1.PLoS ONE,2012,7(11):e49207.
[35]SEO D H,RYU M Y,JAMMES F,HWANG J H,TUREK M,KANGB G,KWAK J M,KIM W T.Roles of Four Arabidopsis U-Box E3ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses.Plant Physiology,2012,160(1):556-568.
[36]YEE D,GORING D R.The diversity of plant U-box E3 ubiquitin ligases:From upstream activators to downstream target substrates.Journal of Experimental Botany,2009,60(4):1109-1121.
[37]WANG M,ZHANG X,LIU J H.Deep sequencing-based characterization of transcriptome of trifoliate orange(Poncirus trifoliata(L.)Raf.)in response to cold stress.BMC Genomics,2015,16(1):555.
[2]刘锴栋,袁长春.泛素/26S蛋白酶体途径及其在植物生长发育中的功能.基因组学与应用生物学,2009,28(6):1219-1228.LIU Y D,YUAN C C.The ubiquitin/26S proteasome pathway and the function in plant development.Genomics and Applied Biology,2009,28(6):1219-1228.(in Chinese)
[3]宋素胜,谢道昕.泛素蛋白酶体途径及其对植物生长发育的调控.植物学通报,2006,23(5):564-577.SONG S S,XIE D X.The ubiquitin-proteosome pathway and plant development.Bulletin of Botany,2006,23(5):564-577.(in Chinese)
[4]VANDEMARK A P,HILL C P.Structural basis of ubiquitylation.Current Opinion Structural Biology,2002,12(6):822-830.
[5]HATAKEYAMA S,YADA M,MATSUMOTO M,ISHIDA N,NAKAYAMA K I.U-box proteins as a new family of ubiquitinprotein ligases.The Journal of Biological Chemistry,2001,276(35):33111-33120.
[6]PATTERSON C.A new gun in town:the U-box is a ubiquitin ligase domain.Science’s STKE,2002,2002(116):pe4.
[7]FARMER L M,BOOK A J,LEE K H,LIN Y L,FU H,VIERSTRA RD.The RAD23 family provides an essential connection between the26S proteasome and ubiquitylated proteins in Arabidopsis.The Plant Cell,2010,22(1):124-142.
[8]VIERSTRA R D.The ubiquitin-26S proteasome system at the nexus of plant biology.Nature Reviews Molecular Cell Biology,2009,10(6):385-397.
[9]GONZALEZ-LAMOTHE R,TSITSIGIANNIS D I,LUDWIG A A,PANICOT M,SHIRASU K,JONES J D G.The U-Box protein CMPG1is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato.Plant Cell,2006,18(4):1067-1083.
[10]CHO S K,CHUNG H S,RYU M Y,PARK M J,LEE M M,BAHK Y,KIM J,PAI H S,KIM W T.Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-box E3 ubiquitin ligases homolog.Plant Physiology,2006,142(4):1664-1682.
[11]LIU Y C,WU Y R,HUANG X H,SUN J,XIE Q.At PUB19,a U-Box E3 ubiquitin ligase,negatively regulates abscisic acid and drought responses in Arabidopsis thaliana.Molecular Plant,2011,4(6):938-946.
[12]HWANG J H,SEO D H,KANG B G,KWAK J M,KIM W T.Suppression of Arabidopsis AtPUB30 resulted in increased tolerance to salt stress during germination.Plant Cell Reports,2015,34(2):277-289.
[13]BRAUMANN I,URBAN W,PREUβA,DOCKTER C,ZAKHRABEKOVA S,HANSSON M.Semi-dwarf barley(Hordeum vulgare L.)brh2 and ari-l mutants are deficient in a U-box E3ubiquitin ligase.Plant Growth Regulation,2018,86(2):223-234.
[14]SAMUEL M A,MUDGIL Y,SALT J N,DELMAS F,RAMACHANDRAN S,CHILELLI A,GORING D R.Interactions between the S-Domain receptor kinases and At PUB-ARM E3ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis.Plant Physiology,2008,147(4):2084-2095.
[15]WU G,TEROL J,IBANEZ V,LOPEZ-GARCIA A,PEREZ-ROMANE,BORREDA C,DOMINGO C,TADEO F R,CARBONELL-CABALLERO J,ALONSO R,CURK F,DU D,OLLITRAULT P,ROOSE M L,DOPAZO J,GMITTER F G,ROKHSAR D S,TALONM.Genomics of the origin and evolution of Citrus.Nature,2018,554(7692):311-316.
[16]郑兴卫,邵麟惠,李聪.蒺藜苜蓿全基因组中U-box基因家族的筛选与特征分析.草业学报,2015,24(8):130-141.ZHENG X W,SHAO L H,LI C.Genome-wide screening and characterization of the U-box gene family in Medicago truncatula.Acta Prataculturase Sinica,2015,24(8):130-141.(in Chinese)
[17]WIBORG J,O'SHEA C,SKRIVER K.Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin-protein ligases.Biochemical Journal,2008,413(3):447-457.
[18]曹英豪.水稻U-box基因家族的特征及转录表达模式分析[D].保定:河北农业大学,2010.CAO Y H.The characteristics of Rice U-Box gene family with its transcription and expression pattern analysis[D].Baoding:Agricultural University of Hebei,2010.(in Chinese)
[19]李菲,何小红,龚记熠.番茄基因组中U-box基因家族的鉴定与分析.分子植物育种.2018,16(11):3468-3476LI F,HE X H,GONG J Y.Identification and analysis of U-box gene family in tomato genome.Molecular Plant Breeding,2018,16(11):3468-3476.(in Chinese)
[20]刘永昌,曾丽亚,盘俊,齐成媚,袁志辉,何福林,胡克坚,刘小文.雷蒙德氏棉Plant U-box(GrPUBs)基因家族生物信息学分析.分子植物育种,2018,16(13):4157-4171.LIU Y C,ZENG L Y,PAN J,QI C M,YUAN Z H,HE F L,HU K J,LIU X W.Bioinformatics analysis of the plant U-box gene families(Gr PUBs)in Gossypium raimondii.Molecular Plant Breeding,2018,16(13):4157-4171.(in Chinese)
[21]IGNACIO M.Ancient origin of animal U-box ubiquitin ligases.BMCEvolutionary Biology,2010,10(1):331.
[22]CONSORTIUM T T G.The tomato genome sequence provides insights into fleshy fruit evolution.Nature,2012,485(7400):635.
[23]LUO J,SHEN G,YAN J,HE C,ZHANG H.At CHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment.The Plant Journal,2006,46(4):649-657.
[24]ADLER G,KONRAD Z,ZAMIR L,MISHRA A K,RAVEH D,BAR-ZVI D.The Arabidopsis paralogs,PUB46 and PUB48,encoding U-box E3 ubiquitin ligases,are essential for plant response to drought stress.BMC Plant Biology,2017,17(1):8.
[25]BERGLER J,HOTH S.Plant U-box armadillo repeat proteins At PUB18 and At PUB19 are involved in salt inhibition of germination in Arabidopsis.Plant Biology,2011,13(5):725-730.
[26]SADANANDOM A.The U-box protein At PUB17 is a functional ortholog of NtACRE276 and its E3 ubiquitin ligase activity is required for plant cell death and defence.Comparative Biochemistry&Physiology Part A,2007,146(4):S203-S203.
[27]SANKARANARAYANAN S,SAMUEL M A.A proposed role for selective autophagy in regulating auxin-dependent lateral root development under phosphate starvation in Arabidopsis.Plant Signaling&Behavior,2015,10(3):e989749.
[28]齐晨辉,赵先炎,韩朋良.苹果U-box型E3泛素连接酶MdPUB24的耐盐性和ABA敏感性鉴定.园艺学报,2017,44(12):2255-2264.QI C H,ZHAO X Y,HAN P L.Functional identification of salt tolerance and ABA sensitivity of apple U-box E3 ubiquitin ligase MdPUB24.Acta Horticulturae Sinica,2017,44(12):2255-2264.(in Chinese)
[29]LIU J,LI W,NING Y,SHIRSEKAR G,CAI Y,WANG X,DAI L,WANG Z,LIU W,WANG G L.The U-Box E3 ligase SPL11/PUB13is a convergence point of defense and flowering signaling in plants.Plant Physiology,2012,160(1):28-37.
[30]SHARMA M,PANDEY G K.Expansion and function of repeat domain proteins during stress and development in plants.Frontiers in Plant Science,2016,6:1218.
[31]SANTNER A,CALDERON-VILLALOBOS L I A,ESTELLE M.Plant hormones are versatile chemical regulators of plant growth.Nature Chemical Biology,2009,5(5):301-307.
[32]HWANG J H,DONG H S,KANG B G,KWAK J M,KIM W T.Suppression of Arabidopsis,At PUB30,resulted in increased tolerance to salt stress during germination.Plant Cell Reports,2015,34(2):277-289.
[33]CHO S K,CHUANG H S,RYU M Y,PARK M J,LEE M M,BAHKY,KIM J,PAI H S,KIM W T.Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-Box E3 ubiquitin ligase homolog.Plant Physiology,2006,142(4):1664-1682.
[34]KOBAYASHI S,TSUGAMA D,LIU S,TAKANO T.A U-Box E3ubiquitin ligase,PUB20,interacts with the Arabidopsis G-Proteinβsubunit,AGB1.PLoS ONE,2012,7(11):e49207.
[35]SEO D H,RYU M Y,JAMMES F,HWANG J H,TUREK M,KANGB G,KWAK J M,KIM W T.Roles of Four Arabidopsis U-Box E3ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses.Plant Physiology,2012,160(1):556-568.
[36]YEE D,GORING D R.The diversity of plant U-box E3 ubiquitin ligases:From upstream activators to downstream target substrates.Journal of Experimental Botany,2009,60(4):1109-1121.
[37]WANG M,ZHANG X,LIU J H.Deep sequencing-based characterization of transcriptome of trifoliate orange(Poncirus trifoliata(L.)Raf.)in response to cold stress.BMC Genomics,2015,16(1):555.