牵牛胁迫应答基因PnLOG2的克隆及功能验证
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摘要
RING型E3泛素连接酶在植物应答非生物胁迫过程中发挥着重要功能。该研究从圆叶牵牛中克隆出RING型E3泛素连接酶基因PnLOG2,该基因序列号为XM_019321049.1。利用ORF Finder预测PnLOG2基因编码开放阅读框长度为912 bp (51～992 bp),编码313个氨基酸,蛋白分子质量34.38 kD,理论等电点为5.14。系统发育分析表明,PnLOG2基因与番茄亲缘关系最近。组织特异性分析表明,PnLOG2基因在牵牛不同组织均有表达,在老茎和新叶中表达量较高。qRT-PCR分析结果表明,PnLOG2基因在圆叶牵牛根和叶中受干旱、盐碱胁迫诱导显著上调表达。通过异源表达PnLOG2基因于酵母细胞中,发现干旱、盐碱胁迫下PnLOG2基因提高了重组酵母的耐盐和耐旱能力,但降低了对碱的耐受性。该研究初步阐明了PnLOG2基因在干旱、盐碱胁迫下的功能,为进一步研究RING型E3泛素连接酶在非生物胁迫中的机理提供了理论依据。
RING type E3 ubiquitin ligase play an important role in plant response to abiotic stress. In this study, we isolated a RING type E3 ubiquitin ligase gene PnLOG2 from Pharbitis purpurea. The gene ID was XM_019321049.1. The length of open reading frame was predicted to be 912 bp(51-992 bp)using ORF Finder. PnLOG2 encoded a protein of 303 residues with a predicted molecular weight of 34.38 kD and an isoelectric point of 5.14. Phylogenetic analysis showed that PnLOG2 gene was clustered with tomato E3 ubiquitin ligase gene. Tissue specific analysis showed that the expression levels of PnLOG2 in different tissues was detected. And the PnLOG2 was highly expressed in the old stem and new leaves. The qRT-PCR data showed that the expression levels of PnLOG2 were significantly inducted by drought, salt and alkali stresses in the roots and leaves of P. purpurea. Further, ectopic expression of PnLOG2 in yeast cells enhanced the tolerance to salt and drought stresses, but decreased the tolerance to alkali stress. Therefore, we identified the function of PnLOG2 gene in response to drought, salt and alkali stresses, and provided a theoretical basis for further study RING-type E3 ubiquitin in abiotic stress.
RING type E3 ubiquitin ligase play an important role in plant response to abiotic stress. In this study, we isolated a RING type E3 ubiquitin ligase gene PnLOG2 from Pharbitis purpurea. The gene ID was XM_019321049.1. The length of open reading frame was predicted to be 912 bp(51-992 bp)using ORF Finder. PnLOG2 encoded a protein of 303 residues with a predicted molecular weight of 34.38 kD and an isoelectric point of 5.14. Phylogenetic analysis showed that PnLOG2 gene was clustered with tomato E3 ubiquitin ligase gene. Tissue specific analysis showed that the expression levels of PnLOG2 in different tissues was detected. And the PnLOG2 was highly expressed in the old stem and new leaves. The qRT-PCR data showed that the expression levels of PnLOG2 were significantly inducted by drought, salt and alkali stresses in the roots and leaves of P. purpurea. Further, ectopic expression of PnLOG2 in yeast cells enhanced the tolerance to salt and drought stresses, but decreased the tolerance to alkali stress. Therefore, we identified the function of PnLOG2 gene in response to drought, salt and alkali stresses, and provided a theoretical basis for further study RING-type E3 ubiquitin in abiotic stress.
引文
[1] YANG L,LIU Q H,LIU Z B,et al.Arabidopsis C3HC4-RING finger E3 ubiquitin ligase AtAIRP4 positively regulates stress-responsive abscisic acid signaling[J].Journal of Integrative Plant Biology,2016,58(1):67-80.
[2] MUNNS R.Comparative physiology of salt and water stress[J].Plant,Cell & Environment,2002,25(2):239-250.
[3] 张冰冰,孙天旭,赵月明,等.羊草LcPIP基因遗传转化露地菊及其抗盐性鉴定[J].植物生理学报,2018,54(3):491-499.ZHANG B B,SUN T X,ZHAO Y M,et al.Genetic transformation of LcPIP gene in Chrysanthemum morifolium and identification of its salt resistance[J].Plant Physiology Journal,2018,54(3):491-499.
[4] GUAN B,ZHOU D,ZHANG H,et al.Germination responses of Medicago ruthenica seeds to salinity,alkalinity,and temperature[J].Journal of Arid Environments,2009,73(1):135-138.
[5] 朱美娇,张海玲,徐香玲,等.泛素/26S蛋白酶体途径调节非生物胁迫的研究进展[J].北方园艺,2015,(3):188-192.ZHU M J,ZHANG H L,XU X L,et al.Research advance in the Ubiquitin/26S proteasome pathway regulating abiotic stress[J].Northern Horticulture,2015,(3):188-192.
[6] DREHER K,CALLIS J.Ubiquitin,hormones and biotic stress in plants[J].Annals of Botany,2007,99(5):787-822.
[7] VIERSTRA R D.The ubiquitin-26S proteasome system at the nexus of plant biology[J].Nature Reviews.Molecular Cell Biology,2009,10(6):385-397.
[8] SANTNER A,ESTELLE M.The ubiquitin-proteasome system regulates plant hormone signaling[J].The Plant Journal:for Cell and Molecular Biology,2010,61(6):1 029-1 040.
[9] SERINO G,XIE Q.The ever expanding role of ubiquitin and SUMO in plant biology[J].Journal of Integrative Plant Biology,2013,55(1):5-6.
[10] ZHANG S C,QI Y L,LIU M,et al.SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana(F)[J].Journal of Integrative Plant Biology,2013,55(1):83-95.
[11] GUERRA D D,CALLIS J.Ubiquitin on the move:The ubiquitin modification system plays diverse roles in the regulation of endoplasmic reticulum-and plasma membrane-localized proteins[J].Plant Physiology,2012,160(1):56-64.
[12] STONE S L,HAUKSDóTTIR H,TROY A,et al.Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis[J].Plant Physiology,2005,137(1):13-30.
[13] STONE S L,CALLIS J.Ubiquitin ligases mediate growth and development by promoting protein death[J].Current Opinion in Plant Biology,2007,10(6):624-632.
[14] GUO L Q,NEZAMES C D,SHENG L X,et al.Cullin-RING ubiquitin ligase family in plant abiotic stress pathways(F).[J].Journal of Integrative Plant Biology,2013,55(1):21-30.
[15] KRAFT E.Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis[J].Plant Physiology,2005,139(4):1 597-1 611.
[16] VIERSTRA R D.The ubiquitin-26S proteasome system at the nexus of plant biology[J].Nature Reviews.Molecular Cell Biology,2009,10(6):385-397.
[17] STONE S L,HAUKSDóTTIR H,TROY A,et al.Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis[J].Plant Physiology,2005,137(1):13-30.
[18] KIM J H,KIM W T.The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses[J].Plant Physiology,2013,162(3):1 733-1 749.
[19] KIM S J,KIM W T.Suppression of Arabidopsis RING E3 ubiquitin ligase AtATL78 increases tolerance to cold stress and decreases tolerance to drought stress[J].FEBS Letters,2013,587(16):2 584-2 590.
[20] ZHANG H W,CUI F,WU Y R,et al.The RING finger ubiquitin E3 ligase SDIR1 targets SDIR1-INTERACTING PROTEIN1 for degradation to modulate the salt stress response and ABA signaling in Arabidopsis[J].The Plant Cell Online,2015,27(1):214-227.
[21] LEE H K,CHO S K,SON O,et al.Drought stress-induced Rma1H1,a RING membrane-anchor E3 ubiquitin ligase homolog,regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants[J].The Plant Cell,2009,21(2):622-641.
[22] 范锡麟,杜强,杨珍珍,等.水稻泛素连接酶基因OsRING6的克隆及表达分析[J].植物遗传资源学报,2016,17(2):337-343.FAN X L,DU Q,YANG Z Z,et al.Cloning and expression analysis of the rice ubiquitin ligase gene OsRING6[J].Journal of Plant Genetic Resources,2016,17(2):337-343.
[23] 孔曼丽,李彩云,孙清鹏,等.玉米E3泛素连接酶类基因ZmGW2-1的克隆及表达分析[J].安徽农业大学学报,2014,41(6):1 004-1 011.KONG M L,LI C Y,SUN Q P,et al.Isolation and expression analysis of the E3 ubiquitin ligase encoding gene ZmGW2-1 in maize[J].Journal of Anhui Agricultural University,2014,41(6):1 004-1 011.
[24] ZHANG X R,GARRETON V,CHUA N H.The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation[J].Genes & Development,2005,19(13):1 532-1 543.
[25] GU X F,JIANG D H,WANG Y Q,et al.Repression of the floral transition via histone H2B monoubiquitination[J].The Plant Journal:for Cell and Molecular Biology,2009,57(3):522-533.
[26] DHAWAN R,LUO H L,FOERSTER A M,et al.HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis[J].The Plant Cell,2009,21(3):1 000-1 019.
[27] SMALLE J,VIERSTRA R D.The ubiquitin 26S proteasome proteolytic pathway[J].Annual Review of Plant Biology,2004,55:555-590.
[28] THOMASHOW M F.PLANT COLD ACCLIMATION:Freezing tolerance genes and regulatory mechanisms[J].Annual Review of Plant Physiology and Plant Molecular Biology,1999,50:571-599.
[29] SHINOZAKI K,YAMAGUCHI-SHINOZAKI K,SEKI M.Regulatory network of gene expression in the drought and cold stress responses[J].Current Opinion in Plant Biology,2003,6(5):410-417.
[30] ZHU J K.Salt and drought stress signal transduction in plants[J].Annual Review of Plant Biology,2002,53:247-273.
[31] 张艳芳,孙瑞芬,郭树春,等.向日葵E3泛素连接酶基因克隆及表达分析[J].西北植物学报,2016,36(10):1 933-1 940.ZHANG Y F,SUN R F,GUO S C,et al.Cloning and expression analysis of E3 ubiquitin ligase gene HERC2 of sunflower (Helianthus annuus L.)[J].Acta Botanica Boreali-Occidentalia Sinica,2016,36(10):1 933-1 940.
[32] 秦岭,杨延兵,陈二影,等.RING-finger类型泛素连接酶E3及其与植物抗旱性的关系[J].分子植物育种,2017,15(7):2 829-2 835.QIN L,YANG Y B,CHEN E Y,et al.RING-finger type ubiquitin ligase E3 and its relationship with the plant drought resistance in plants[J].Molecular Plant Breeding,2017,15(7):2 829-2 835.
[33] JOO H,LIM C W,LEE S C.Identification and functional expression of the pepper RING type E3 ligase,CaDTR1,involved in drought stress tolerance via ABA-mediated signalling[J].Scientific Reports,2016,6:30 097.
[34] SADHUKHAN A,PANDA S K,SAHOO L.The cowpea RING ubiquitin ligase VuDRIP interacts with transcription factor VuDREB2A for regulating abiotic stress responses[J].Plant Physiology and Biochemistry:PPB,2014,83:51-56.
[35] DU Q L,CUI W Z,ZHANG C H,et al.GmRFP1 encodes a previously unknown RING-type E3 ubiquitin ligase in Soybean (Glycine max)[J].Molecular Biology Reports,2010,37(2):685-693.
[36] SUN X L,SUN M Z,LUO X,et al.A Glycine soja ABA-responsive receptor-like cytoplasmic kinase,GsRLCK,positively controls plant tolerance to salt and drought stresses[J].Planta,2013,237(6):1 527-1 545.
[37] ZHANG Y Y,YANG C W,LI Y,et al.SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis[J].The Plant Cell,2007,19(6):1 912-1 929.
[38] GAO T,WU Y R,ZHANG Y Y,et al.OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice[J].Plant Molecular Biology,2011,76(1-2):145-156.
[39] RYU M Y,CHO S K,KIM W T.The Arabidopsis C3H2C3-type RING E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress[J].Plant Physiology,2010,154(4):1 983-1 997.
[40] LI H M,JIANG H L,BU Q Y,et al.The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response[J].Plant Physiology,2011,156(2):550-563.
[41] KO J H,YANG S H,HAN K H.Upregulation of an Arabidopsis RING-H2 gene,XERICO,confers drought tolerance through increased abscisic acid biosynthesis[J].The Plant Journal,2006,47(3):343-355.
[42] KIM S J,RYU M Y,KIM W T.Suppression of Arabidopsis RING-DUF1117 E3 ubiquitin ligases,AtRDUF1 and AtRDUF2,reduces tolerance to ABA-mediated drought stress[J].Biochemical and Biophysical Research Communications,2012,420(1):141-147.
[43] CHENG M C,HSIEH E J,CHEN J H,et al.CORRECTION.Arabidopsis RGLG2,functioning as a RING E3 ligase,interacts with AtERF53 and negatively regulates the plant drought stress response[J].Plant Physiology,2016,170(2):1 162-1 163.
[44] NING Y S,JANTASURIYARAT C,ZHAO Q Z,et al.The SINA E3 ligase OsDIS1 negatively regulates drought response in rice[J].Plant Physiology,2011,157(1):242-255.
[45] JU H W,MIN J H,CHUNG M S,et al.The atrzf1 mutation of the novel RING-type E3 ubiquitin ligase increases proline contents and enhances drought tolerance in Arabidopsis[J].Plant Science,2013,203-204:1-7.
[46] LIM C W,PARK C,KIM J H,et al.Pepper CaREL1,a ubiquitin E3 ligase,regulates drought tolerance via the ABA-signalling pathway[J].Scientific Reports,2017,7:477.
[47] LIU J P,ZHANG C C,WEI C C,et al.The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice[J].Plant Physiology,2016,170(1):429-443.
[48] QI S L,LIN Q F,ZHU H S,et al.The RING finger E3 ligase SpRing is a positive regulator of salt stress signaling in salt-tolerant wild tomato species[J].Plant & Cell Physiology,2016,57(3):528-539.
[49] AN J P,LIU X,SONG L Q,et al.Apple RING finger E3 ubiquitin ligase MdMIEL1 negatively regulates salt and oxidative stresses tolerance[J].Journal of Plant Biology,2017,60(2):137-145.
[50] 刘彩霞.柽柳ThTIP和ThDUF106基因的遗传转化及功能分析[D].哈尔滨:东北林业大学,2017.
[2] MUNNS R.Comparative physiology of salt and water stress[J].Plant,Cell & Environment,2002,25(2):239-250.
[3] 张冰冰,孙天旭,赵月明,等.羊草LcPIP基因遗传转化露地菊及其抗盐性鉴定[J].植物生理学报,2018,54(3):491-499.ZHANG B B,SUN T X,ZHAO Y M,et al.Genetic transformation of LcPIP gene in Chrysanthemum morifolium and identification of its salt resistance[J].Plant Physiology Journal,2018,54(3):491-499.
[4] GUAN B,ZHOU D,ZHANG H,et al.Germination responses of Medicago ruthenica seeds to salinity,alkalinity,and temperature[J].Journal of Arid Environments,2009,73(1):135-138.
[5] 朱美娇,张海玲,徐香玲,等.泛素/26S蛋白酶体途径调节非生物胁迫的研究进展[J].北方园艺,2015,(3):188-192.ZHU M J,ZHANG H L,XU X L,et al.Research advance in the Ubiquitin/26S proteasome pathway regulating abiotic stress[J].Northern Horticulture,2015,(3):188-192.
[6] DREHER K,CALLIS J.Ubiquitin,hormones and biotic stress in plants[J].Annals of Botany,2007,99(5):787-822.
[7] VIERSTRA R D.The ubiquitin-26S proteasome system at the nexus of plant biology[J].Nature Reviews.Molecular Cell Biology,2009,10(6):385-397.
[8] SANTNER A,ESTELLE M.The ubiquitin-proteasome system regulates plant hormone signaling[J].The Plant Journal:for Cell and Molecular Biology,2010,61(6):1 029-1 040.
[9] SERINO G,XIE Q.The ever expanding role of ubiquitin and SUMO in plant biology[J].Journal of Integrative Plant Biology,2013,55(1):5-6.
[10] ZHANG S C,QI Y L,LIU M,et al.SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana(F)[J].Journal of Integrative Plant Biology,2013,55(1):83-95.
[11] GUERRA D D,CALLIS J.Ubiquitin on the move:The ubiquitin modification system plays diverse roles in the regulation of endoplasmic reticulum-and plasma membrane-localized proteins[J].Plant Physiology,2012,160(1):56-64.
[12] STONE S L,HAUKSDóTTIR H,TROY A,et al.Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis[J].Plant Physiology,2005,137(1):13-30.
[13] STONE S L,CALLIS J.Ubiquitin ligases mediate growth and development by promoting protein death[J].Current Opinion in Plant Biology,2007,10(6):624-632.
[14] GUO L Q,NEZAMES C D,SHENG L X,et al.Cullin-RING ubiquitin ligase family in plant abiotic stress pathways(F).[J].Journal of Integrative Plant Biology,2013,55(1):21-30.
[15] KRAFT E.Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis[J].Plant Physiology,2005,139(4):1 597-1 611.
[16] VIERSTRA R D.The ubiquitin-26S proteasome system at the nexus of plant biology[J].Nature Reviews.Molecular Cell Biology,2009,10(6):385-397.
[17] STONE S L,HAUKSDóTTIR H,TROY A,et al.Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis[J].Plant Physiology,2005,137(1):13-30.
[18] KIM J H,KIM W T.The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses[J].Plant Physiology,2013,162(3):1 733-1 749.
[19] KIM S J,KIM W T.Suppression of Arabidopsis RING E3 ubiquitin ligase AtATL78 increases tolerance to cold stress and decreases tolerance to drought stress[J].FEBS Letters,2013,587(16):2 584-2 590.
[20] ZHANG H W,CUI F,WU Y R,et al.The RING finger ubiquitin E3 ligase SDIR1 targets SDIR1-INTERACTING PROTEIN1 for degradation to modulate the salt stress response and ABA signaling in Arabidopsis[J].The Plant Cell Online,2015,27(1):214-227.
[21] LEE H K,CHO S K,SON O,et al.Drought stress-induced Rma1H1,a RING membrane-anchor E3 ubiquitin ligase homolog,regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants[J].The Plant Cell,2009,21(2):622-641.
[22] 范锡麟,杜强,杨珍珍,等.水稻泛素连接酶基因OsRING6的克隆及表达分析[J].植物遗传资源学报,2016,17(2):337-343.FAN X L,DU Q,YANG Z Z,et al.Cloning and expression analysis of the rice ubiquitin ligase gene OsRING6[J].Journal of Plant Genetic Resources,2016,17(2):337-343.
[23] 孔曼丽,李彩云,孙清鹏,等.玉米E3泛素连接酶类基因ZmGW2-1的克隆及表达分析[J].安徽农业大学学报,2014,41(6):1 004-1 011.KONG M L,LI C Y,SUN Q P,et al.Isolation and expression analysis of the E3 ubiquitin ligase encoding gene ZmGW2-1 in maize[J].Journal of Anhui Agricultural University,2014,41(6):1 004-1 011.
[24] ZHANG X R,GARRETON V,CHUA N H.The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation[J].Genes & Development,2005,19(13):1 532-1 543.
[25] GU X F,JIANG D H,WANG Y Q,et al.Repression of the floral transition via histone H2B monoubiquitination[J].The Plant Journal:for Cell and Molecular Biology,2009,57(3):522-533.
[26] DHAWAN R,LUO H L,FOERSTER A M,et al.HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis[J].The Plant Cell,2009,21(3):1 000-1 019.
[27] SMALLE J,VIERSTRA R D.The ubiquitin 26S proteasome proteolytic pathway[J].Annual Review of Plant Biology,2004,55:555-590.
[28] THOMASHOW M F.PLANT COLD ACCLIMATION:Freezing tolerance genes and regulatory mechanisms[J].Annual Review of Plant Physiology and Plant Molecular Biology,1999,50:571-599.
[29] SHINOZAKI K,YAMAGUCHI-SHINOZAKI K,SEKI M.Regulatory network of gene expression in the drought and cold stress responses[J].Current Opinion in Plant Biology,2003,6(5):410-417.
[30] ZHU J K.Salt and drought stress signal transduction in plants[J].Annual Review of Plant Biology,2002,53:247-273.
[31] 张艳芳,孙瑞芬,郭树春,等.向日葵E3泛素连接酶基因克隆及表达分析[J].西北植物学报,2016,36(10):1 933-1 940.ZHANG Y F,SUN R F,GUO S C,et al.Cloning and expression analysis of E3 ubiquitin ligase gene HERC2 of sunflower (Helianthus annuus L.)[J].Acta Botanica Boreali-Occidentalia Sinica,2016,36(10):1 933-1 940.
[32] 秦岭,杨延兵,陈二影,等.RING-finger类型泛素连接酶E3及其与植物抗旱性的关系[J].分子植物育种,2017,15(7):2 829-2 835.QIN L,YANG Y B,CHEN E Y,et al.RING-finger type ubiquitin ligase E3 and its relationship with the plant drought resistance in plants[J].Molecular Plant Breeding,2017,15(7):2 829-2 835.
[33] JOO H,LIM C W,LEE S C.Identification and functional expression of the pepper RING type E3 ligase,CaDTR1,involved in drought stress tolerance via ABA-mediated signalling[J].Scientific Reports,2016,6:30 097.
[34] SADHUKHAN A,PANDA S K,SAHOO L.The cowpea RING ubiquitin ligase VuDRIP interacts with transcription factor VuDREB2A for regulating abiotic stress responses[J].Plant Physiology and Biochemistry:PPB,2014,83:51-56.
[35] DU Q L,CUI W Z,ZHANG C H,et al.GmRFP1 encodes a previously unknown RING-type E3 ubiquitin ligase in Soybean (Glycine max)[J].Molecular Biology Reports,2010,37(2):685-693.
[36] SUN X L,SUN M Z,LUO X,et al.A Glycine soja ABA-responsive receptor-like cytoplasmic kinase,GsRLCK,positively controls plant tolerance to salt and drought stresses[J].Planta,2013,237(6):1 527-1 545.
[37] ZHANG Y Y,YANG C W,LI Y,et al.SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis[J].The Plant Cell,2007,19(6):1 912-1 929.
[38] GAO T,WU Y R,ZHANG Y Y,et al.OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice[J].Plant Molecular Biology,2011,76(1-2):145-156.
[39] RYU M Y,CHO S K,KIM W T.The Arabidopsis C3H2C3-type RING E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress[J].Plant Physiology,2010,154(4):1 983-1 997.
[40] LI H M,JIANG H L,BU Q Y,et al.The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response[J].Plant Physiology,2011,156(2):550-563.
[41] KO J H,YANG S H,HAN K H.Upregulation of an Arabidopsis RING-H2 gene,XERICO,confers drought tolerance through increased abscisic acid biosynthesis[J].The Plant Journal,2006,47(3):343-355.
[42] KIM S J,RYU M Y,KIM W T.Suppression of Arabidopsis RING-DUF1117 E3 ubiquitin ligases,AtRDUF1 and AtRDUF2,reduces tolerance to ABA-mediated drought stress[J].Biochemical and Biophysical Research Communications,2012,420(1):141-147.
[43] CHENG M C,HSIEH E J,CHEN J H,et al.CORRECTION.Arabidopsis RGLG2,functioning as a RING E3 ligase,interacts with AtERF53 and negatively regulates the plant drought stress response[J].Plant Physiology,2016,170(2):1 162-1 163.
[44] NING Y S,JANTASURIYARAT C,ZHAO Q Z,et al.The SINA E3 ligase OsDIS1 negatively regulates drought response in rice[J].Plant Physiology,2011,157(1):242-255.
[45] JU H W,MIN J H,CHUNG M S,et al.The atrzf1 mutation of the novel RING-type E3 ubiquitin ligase increases proline contents and enhances drought tolerance in Arabidopsis[J].Plant Science,2013,203-204:1-7.
[46] LIM C W,PARK C,KIM J H,et al.Pepper CaREL1,a ubiquitin E3 ligase,regulates drought tolerance via the ABA-signalling pathway[J].Scientific Reports,2017,7:477.
[47] LIU J P,ZHANG C C,WEI C C,et al.The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice[J].Plant Physiology,2016,170(1):429-443.
[48] QI S L,LIN Q F,ZHU H S,et al.The RING finger E3 ligase SpRing is a positive regulator of salt stress signaling in salt-tolerant wild tomato species[J].Plant & Cell Physiology,2016,57(3):528-539.
[49] AN J P,LIU X,SONG L Q,et al.Apple RING finger E3 ubiquitin ligase MdMIEL1 negatively regulates salt and oxidative stresses tolerance[J].Journal of Plant Biology,2017,60(2):137-145.
[50] 刘彩霞.柽柳ThTIP和ThDUF106基因的遗传转化及功能分析[D].哈尔滨:东北林业大学,2017.