菊花AINTEGUMENTA克隆与功能分析
|
摘要
【目的】从菊花中分离克隆AINTEGUMENTA,分析其序列特征和在菊花中的时空表达特性,通过基因沉默研究其对菊花花序发育的影响,分析可能的调控方式和潜在机理,为菊花花序大小的调控奠定理论基础。【方法】使用RACE方法从菊花中克隆AINTEGUMENTA全长,通过DNAMAN等软件对其序列进行分析。采用荧光定量的方式检测其在菊花不同器官和发育时期的表达。构建35S::CmANT-GFP融合蛋白载体进行亚细胞定位,构建TRV2-CmANT沉默表达载体侵染菊花。使用SPSS软件统计分析CmANT沉默系菊花表型变化,通过光学显微镜观察舌状花花瓣表皮细胞变化,使用荧光定量方式检测CmANT相关基因在沉默系中的表达。【结果】从菊花中克隆了CmANT全长,其编码的氨基酸序列长度为540,理论等电点为7.39,蛋白质的理论分子量为60.4 k D,含有两个AP2保守功能区域和VYL修饰位点。在与其他物种的ANT蛋白构建的系统进化树中,CmANT与At ANT聚在一起。荧光定量结果表明:(1)CmANT在花蕾中的表达量最高,其次是根>茎>叶。(2)在花序不同部位的比较中,舌状花中的表达量最高,其次是筒状花,在花萼中的表达量最低。(3)CmANT在舌状花中的表达随着发育时期的延续而降低。(4)CmANT在2,4-D诱导下的3—6 h内表达量持续上升。Wo LF PSORT软件预测和35S::CmANT-GFP融合蛋白在洋葱表皮细胞中的定位结果显示,CmANT蛋白定位在植物细胞核中。TRV-CmANT-1和TRV-CmANT-2沉默系的平均花径相比对照分别减小18.93%和27.47%,舌状花的数目分别减少11.39%和14.66%,其中TRV-CmANT-2与对照差异显著(P<0.05),筒状花数目分别减少14.55%和36.56%。顶端花序的舌状花平均长度分别减少34.17%和54.68%,舌状花的宽度分别比对照减小24.05%和10.13%。叶片平均鲜重分别比对照组减小13.19%和21.98%,叶片鲜重与筒状花数目显著相关(P<0.05)。舌状花花瓣表皮细胞显微观察发现,沉默系舌状花花瓣表皮细胞长度和宽度与对照差异不明显。CmLAX3在两沉默系中的表达明显上升,在小花原基分化期时分别是对照中的1.8和1.78倍,同期CmCYCD3的表达分别下降了32.28%和38.19%,CmXTH4和CmEXPA1的表达量在多个时期也明显降低。【结论】根据沉默系表型与相关基因的表达,推测CmANT的沉默可能解除了对CmLAX3抑制,促进了生长素的转运和过量积累,间接抑制了CmCYCD3的活性,限制了细胞的分裂增殖,引发细胞数目变少,导致沉默系器官变小。
【Objective】 To understand the role of AINTEGUMENTA gene in chrysanthemum inflorescence development, we cloned AINTEGUMENTA gene from chrysanthemum, analyzed its sequence, and characterized its temporal and spatial expression pattern. We further analyzed the impact of AINTEGUMENTA silence on inflorescence development and its possible regulation mode. This study was carried to reveal the potential mechanism of AINTEGUMENTA in governing inflorescence development, which in turn can provide a theoretical basis for chrysanthemum inflorescence diameter adjustment. 【Method】 The chrysanthemum AINTEGUMENTA gene was cloned by RACE method and its sequence was analyzed with DANMAN software. Its expression in different developmental stages and organs of chrysanthemum was detected by real-time fluorescent quantitation PCR. The plasmid of 35 S::CmANT-GFP was constructed for the subcellular localization. The silence vector of TRV2-CmANT was constructed to infect chrysanthemums. The statistics of phenotypic changes in CmANT silenced chrysanthemums were analyzed via SPSS software. The ray florets petal epithelial cells were observed with optical microscope. The expression of CmANT and related genes were detected by real-time fluorescent quantitation PCR. 【Result】 The full-length of CmANT was cloned from chrysanthemum. It encodes 540 amino acids and contains two AP2 conserved function domains and VYL modification sites. The theoretical isoelectric point of CmANT is 7.39 and its molecular weight is 60.4 k D. The phylogenetic tree composed of ANT proteins from various plants species showed that CmANT and Aa ANT had been grouped together. The real-time fluorescent quantitation results showed that:(1) CmANT was expressed most in floral buds, followed by roots, stems and leaves.(2) Gene expression in different parts of inflorescence indicated that CmANT was expressed the most in ray florets followed tubular florets and the lowest in the sepal.(3) The expression of CmANT declined during the development of ray florets.(4) The expression of CmANT under 2,4-D treatment increased between 3 h to 6 h. Wo LF PSORT prediction and 35 S::CmANT-GFP fusion protein localization in onion epithelial cells indicated that CmANT protein was located in cell nucleus. Compared with the control, the mean inflorescence diameters of chrysanthemums in TRV-CmANT-1 and TRV-CmANT-2 lines were decreased by 18.93% and 27.47% respectively and the numbers of ray florets were decreased by 11.39% and 14.66% respectively, among which the difference between TRV-CmANT-2 lines and the control was statistically significant(P<0.05). The numbers of tubular florets were decreased by 14.55% and 36.56%, the mean length of ray florets in top inflorescences was decreased by 34.17% and 54.68%, and the width was decreased by 24.05% and 10.13% respectively in TRV-CmANT-1 and TRV-CmANT-2 lines compared with the control, the mean fresh weight of leaves was decreased by 13.19% and 21.98% respectively in TRV-CmANT-1 and TRV-CmANT-2 lines and the correlation between leaf fresh weight and tubular floret number was significant(P<0.05). The microscopic observation of epithelial cells in ray floret petals indicated that the cell length and width of petals in the silenced lines and the control had no visible differences. The expression of CmLAX3 in two silenced chrysanthemums lines were 1.8 and 1.78 times higher than the control, respectively. Meanwhile the expression of CmCYCD3 was decreased by 32.28% and 38.19% in two silenced lines and the expression of CmXTH4 and CmEXPA1 also decreased at most developmental stages. 【Conclusion】 Due to the phenotypic changes and CmANT expression pattern in silenced chrysanthemums lines, we speculated that the silence of CmANT might relieve the repression on CmLAX3, facilitate the transport and accumulation of auxins, indirectly repress the activation of CmCYCD3, limit the cell division, and cause the decrease of cell number, combined of which would eventually lead to the smaller organ sizes in silenced chrysanthemums lines.
【Objective】 To understand the role of AINTEGUMENTA gene in chrysanthemum inflorescence development, we cloned AINTEGUMENTA gene from chrysanthemum, analyzed its sequence, and characterized its temporal and spatial expression pattern. We further analyzed the impact of AINTEGUMENTA silence on inflorescence development and its possible regulation mode. This study was carried to reveal the potential mechanism of AINTEGUMENTA in governing inflorescence development, which in turn can provide a theoretical basis for chrysanthemum inflorescence diameter adjustment. 【Method】 The chrysanthemum AINTEGUMENTA gene was cloned by RACE method and its sequence was analyzed with DANMAN software. Its expression in different developmental stages and organs of chrysanthemum was detected by real-time fluorescent quantitation PCR. The plasmid of 35 S::CmANT-GFP was constructed for the subcellular localization. The silence vector of TRV2-CmANT was constructed to infect chrysanthemums. The statistics of phenotypic changes in CmANT silenced chrysanthemums were analyzed via SPSS software. The ray florets petal epithelial cells were observed with optical microscope. The expression of CmANT and related genes were detected by real-time fluorescent quantitation PCR. 【Result】 The full-length of CmANT was cloned from chrysanthemum. It encodes 540 amino acids and contains two AP2 conserved function domains and VYL modification sites. The theoretical isoelectric point of CmANT is 7.39 and its molecular weight is 60.4 k D. The phylogenetic tree composed of ANT proteins from various plants species showed that CmANT and Aa ANT had been grouped together. The real-time fluorescent quantitation results showed that:(1) CmANT was expressed most in floral buds, followed by roots, stems and leaves.(2) Gene expression in different parts of inflorescence indicated that CmANT was expressed the most in ray florets followed tubular florets and the lowest in the sepal.(3) The expression of CmANT declined during the development of ray florets.(4) The expression of CmANT under 2,4-D treatment increased between 3 h to 6 h. Wo LF PSORT prediction and 35 S::CmANT-GFP fusion protein localization in onion epithelial cells indicated that CmANT protein was located in cell nucleus. Compared with the control, the mean inflorescence diameters of chrysanthemums in TRV-CmANT-1 and TRV-CmANT-2 lines were decreased by 18.93% and 27.47% respectively and the numbers of ray florets were decreased by 11.39% and 14.66% respectively, among which the difference between TRV-CmANT-2 lines and the control was statistically significant(P<0.05). The numbers of tubular florets were decreased by 14.55% and 36.56%, the mean length of ray florets in top inflorescences was decreased by 34.17% and 54.68%, and the width was decreased by 24.05% and 10.13% respectively in TRV-CmANT-1 and TRV-CmANT-2 lines compared with the control, the mean fresh weight of leaves was decreased by 13.19% and 21.98% respectively in TRV-CmANT-1 and TRV-CmANT-2 lines and the correlation between leaf fresh weight and tubular floret number was significant(P<0.05). The microscopic observation of epithelial cells in ray floret petals indicated that the cell length and width of petals in the silenced lines and the control had no visible differences. The expression of CmLAX3 in two silenced chrysanthemums lines were 1.8 and 1.78 times higher than the control, respectively. Meanwhile the expression of CmCYCD3 was decreased by 32.28% and 38.19% in two silenced lines and the expression of CmXTH4 and CmEXPA1 also decreased at most developmental stages. 【Conclusion】 Due to the phenotypic changes and CmANT expression pattern in silenced chrysanthemums lines, we speculated that the silence of CmANT might relieve the repression on CmLAX3, facilitate the transport and accumulation of auxins, indirectly repress the activation of CmCYCD3, limit the cell division, and cause the decrease of cell number, combined of which would eventually lead to the smaller organ sizes in silenced chrysanthemums lines.
引文
[1]MIZOI J,SHINOZAKI K,YAMAGUCHI-SHINOZAKI K.AP2/ERF family transcription factors in plant abiotic stress responses.Biochimica et Biophysica Acta(BBA)-Bioenergetics,2012,1819(2):86-96.
[2]KRIZEK B A.AINTEGUMENTA-LIKE genes have partly overlapping functions with AINTEGUMENTA but make distinct contributions to Arabidopsis thaliana flower development.Journal of Experimental Botany,2015,66(15):4537-4549.
[3]ZUMAJO-CARDONA C,PABóN-MORA N.Evolution of the APETALA2 gene lineage in seed plants.Molecular Biology and Evolution,2016,33(7):1818-1832.
[4]HORSTMAN A,WILLEMSEN V,BOUTILIER K,HEIDSTRA R.AINTEGUMENTA-LIKE proteins:Hubs in a plethora of networks.Trends in Plant Science,2014,19(3):146-157.
[5]MUDUNKOTHGE J S,KRIZEK B A.Three Arabidopsis AIL/PLT genes act in combination to regulate shoot apical meristem function.The Plant Journal,2012,71(1):108-121.
[6]ELLIOTT R C,BETZNER A S,HUTTNER E,OAKES M P,TUCKER W,GERENTES D,PEREZ P,SMYTH D R.AINTEGUMENTA,an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth.The Plant Cell,1996,8(2):155-168.
[7]KLUCHER K M,CHOW H,REISER L,FISCHER R L.The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2.The Plant Cell,1996,8(2):137-153.
[8]MIZUKAMI Y,FISCHER R L.Plant organ size control:AINTEGUMENTA regulates growth and cell numbers during organogenesis.Proceedings of the National Academy of Sciences of the USA,2000,97(2):942-947.
[9]KRIZEK B,BEQUETTE C,XU K,BLAKLEY I,FU Z,STRATMANN J,LORAINE A.RNA-Seq links the transcription factors AINTEGUMENTA and AINTEGUMENTA-LIKE6 to cell wall remodeling and plant defense pathways.Plant Physiology,2016,171(3):2069-84.
[10]YAMAGUCHI N,JEONG C W,NOLE-WILSON S,KRIZEK B A,WAGNER D.AINTEGUMENTA and AINTEGUMENTA-LIKE6/PLETHORA3 induce LEAFY expression in response to auxin to promote the onset of flower formation in Arabidopsis.Plant Physiology,2016,170(1):283-293.
[11]HU Y,XIE Q,CHUA N H.The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size.The Plant Cell,2003,15(9):1951-1961.
[12]KRIZEK B A.Aintegumenta and Aintegumenta-Like6 regulate auxin-mediated flower development in Arabidopsis.BMC Research Notes,2011,4(1):176.
[13]KRIZEK B A.Auxin regulation of Arabidopsis flower development involves members of the AINTEGUMENTA-LIKE/PLETHORA(AIL/PLT)family.Journal of Experimental Botany,2011,62(10):3311-3319.
[14]CHIALVA C,EICHLER E,GRISSI C,MU?OZ C,GOMEZTALQUENCA S,MARTíNEZ-ZAPATER J M,LIJAVETZKY D.Expression of grapevine AINTEGUMENTA-like genes is associated with variation in ovary and berry size.Plant Molecular Biology,2016:1-14.
[15]SMACZNIAK C,IMMINK R G H,MUI?O J M,BLANVILLAIN R,BUSSCHER M,BUSSCHER-LANGE J,DINH Q D,LIU S,WESTPHAL A H,BOEREN S,PARCY F,XU L,CARLES C C,ANGENENT G C,KAUFMANN K.Characterization of MADSdomain transcription factor complexes in Arabidopsis flower development.Proceedings of the National Academy of Sciences of the USA,2012,109(5):1560-1565.
[16]DEWITTE W,RIOU-KHAMLICHI C,SCOFIELD S,HEALY J,JACQMARD A,KILBY N,MURRAY J.Altered cell cycle distribution,hyperplasia,and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3.Plant Cell,2003,15(1):79-92.
[17]HARADA T,TORII Y,MORITA S,ONODERA R,HARA Y,YOKOYAMA R,NISHITANI K,SATOH S.Cloning,characterization,and expression of xyloglucan endotransglucosylase/hydrolase and expansin genes associated with petal growth and development during carnation flower opening.Journal Of Experimental Botany,2011,62(2):815-823.
[18]YAMAGUCHI N,WU M-F,WINTER C M,BERNS M C,NOLE-WILSON S,YAMAGUCHI A,COUPLAND G,KRIZEK B A,WAGNER D.A molecular framework for auxin-mediated initiation of flower primordia.Developmental Cell,2013,24(3):271-282.
[19]LüP,ZHANG C,LIU J,LIU X,JIANG G,JIANG X,KHAN M A,WANG L,HONG B,GAO J.Rh HB1 mediates the antagonism of gibberellins to ABA and ethylene during rose(Rosa hybrida)petal senescence.The Plant Journal,2014,78(4):578-590.
[20]杨娜,郭维明,陈发棣,房伟民.光周期对秋菊品种’神马’花芽分化和开花的影响.园艺学报,2007,34(4):965-972.YANG N,GUO W M,CHEN F D,FANG W M.Effects of photoperiod on floral bud differentiation and flowering of Chrysanthemum morifolium Ramat.‘Jinba’.Acta Horticulturae Sinica,2007,34(4):965-972.(in Chinese)
[21]JOFUKU K D,DEN BOER B,VAN MONTAGU M,OKAMURO J K.Control of Arabidopsis flower and seed development by the homeotic gene APETALA2.The Plant Cell,1994,6(9):1211-1225.
[22]KRIZEK B A.AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain.Nucleic Acids Research,2003,31(7):1859-1868.
[23]MASAKI T,MITSUI N,TSUKAGOSHI H,NISHII T,MORIKAMI A,NAKAMURA K.ACTIVATOR of Spomin::LUC1/WRINKLED1of Arabidopsis thaliana Transactivates Sugar-inducible Promoters.Plant and Cell Physiology,2005,46(4):547-556.
[24]NOLE-WILSON S,KRIZEK B A.DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA.Nucleic Acids Research,2000,28(21):4076-4082.
[25]盛慧,秦智伟,李文滨,周秀艳,武涛,辛明.黄瓜生长素反应因子(ARF)家族鉴定及表达特异性分析.中国农业科学,2014,47(10):1985-1994.SHENG H,QIN Z W,LI W B,ZHOU X Y,WU T,XIN M.Genome-wide identification and expression analysis of auxin response factor(ARF)family in cucumber.Scientia Agricultura Sinica,2014,47(10):1985-1994.(in Chinese)
[26]MüLLER B,SHEEN J.Cytokinin and auxin interplay in root stem-cell specification during early embryogenesis.Nature,2008,453(7198):1094-1097.
[27]NOLE-WILSON S,TRANBY T L,KRIZEK B A.AINTEGUMENTAlike(AIL)genes are expressed in young tissues and may specify meristematic or division-competent states.Plant Molecular Biology,2005,57(5):613-628.
[28]MENGES M,SAMLAND A,PLANCHAIS S,MURRAY J.The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis.Plant Cell,2006,18(4):893-906.
[29]RANDALL R,SORNAY E,DEWITTE W,MURRAY J.AINTEGUMENTA and the D-type cyclin CYCD3;1 independently contribute to petal size control in Arabidopsis:evidence for organ size compensation being an emergent rather than a determined property.Journal of Experimental Botany,2015,66(13):3991-4000.
[30]PORCO S,LARRIEU A,DU Y,GAUDINIER A,GOH T,SWARUP K,SWARUP R,KUEMPERS B,BISHOPP A,LAVENUS J,CASIMIRO I,HILL K,BENKOVA E,FUKAKI H,BRADY S,SCHERES B,PéRET B,BENNETT M.Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3.Development,2016,143(18):3340-3349.
[31]GARZA-AGUILAR S,LARA-Nú?EZ A,GARCíA-RAMíREZ E,VáZQUEZ-RAMOS J.Modulation of Cyc D3;1-CDK complexes by phytohormones and sucrose during maize germination.Physiologia Plantarum,2017,160(1):84-97.
[32]VANDENBUSSCHE F,PETRáSEK J,ZáDNíKOVáP,HOYEROVáK,PESEK B,RAZ V,SWARUP R,BENNETT M,ZAZíMALOVáE,BENKOVáE,VAN DER STRAETEN D.The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings.Development,2010,137(4):597-606.
[33]PEAUCELLE A,BRAYBROOK S,LE GUILLOU L,BRON E,KUHLEMEIER C,H?FTE H.Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis.Current Biology,2011,21(20):1720-1726.
[2]KRIZEK B A.AINTEGUMENTA-LIKE genes have partly overlapping functions with AINTEGUMENTA but make distinct contributions to Arabidopsis thaliana flower development.Journal of Experimental Botany,2015,66(15):4537-4549.
[3]ZUMAJO-CARDONA C,PABóN-MORA N.Evolution of the APETALA2 gene lineage in seed plants.Molecular Biology and Evolution,2016,33(7):1818-1832.
[4]HORSTMAN A,WILLEMSEN V,BOUTILIER K,HEIDSTRA R.AINTEGUMENTA-LIKE proteins:Hubs in a plethora of networks.Trends in Plant Science,2014,19(3):146-157.
[5]MUDUNKOTHGE J S,KRIZEK B A.Three Arabidopsis AIL/PLT genes act in combination to regulate shoot apical meristem function.The Plant Journal,2012,71(1):108-121.
[6]ELLIOTT R C,BETZNER A S,HUTTNER E,OAKES M P,TUCKER W,GERENTES D,PEREZ P,SMYTH D R.AINTEGUMENTA,an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth.The Plant Cell,1996,8(2):155-168.
[7]KLUCHER K M,CHOW H,REISER L,FISCHER R L.The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2.The Plant Cell,1996,8(2):137-153.
[8]MIZUKAMI Y,FISCHER R L.Plant organ size control:AINTEGUMENTA regulates growth and cell numbers during organogenesis.Proceedings of the National Academy of Sciences of the USA,2000,97(2):942-947.
[9]KRIZEK B,BEQUETTE C,XU K,BLAKLEY I,FU Z,STRATMANN J,LORAINE A.RNA-Seq links the transcription factors AINTEGUMENTA and AINTEGUMENTA-LIKE6 to cell wall remodeling and plant defense pathways.Plant Physiology,2016,171(3):2069-84.
[10]YAMAGUCHI N,JEONG C W,NOLE-WILSON S,KRIZEK B A,WAGNER D.AINTEGUMENTA and AINTEGUMENTA-LIKE6/PLETHORA3 induce LEAFY expression in response to auxin to promote the onset of flower formation in Arabidopsis.Plant Physiology,2016,170(1):283-293.
[11]HU Y,XIE Q,CHUA N H.The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size.The Plant Cell,2003,15(9):1951-1961.
[12]KRIZEK B A.Aintegumenta and Aintegumenta-Like6 regulate auxin-mediated flower development in Arabidopsis.BMC Research Notes,2011,4(1):176.
[13]KRIZEK B A.Auxin regulation of Arabidopsis flower development involves members of the AINTEGUMENTA-LIKE/PLETHORA(AIL/PLT)family.Journal of Experimental Botany,2011,62(10):3311-3319.
[14]CHIALVA C,EICHLER E,GRISSI C,MU?OZ C,GOMEZTALQUENCA S,MARTíNEZ-ZAPATER J M,LIJAVETZKY D.Expression of grapevine AINTEGUMENTA-like genes is associated with variation in ovary and berry size.Plant Molecular Biology,2016:1-14.
[15]SMACZNIAK C,IMMINK R G H,MUI?O J M,BLANVILLAIN R,BUSSCHER M,BUSSCHER-LANGE J,DINH Q D,LIU S,WESTPHAL A H,BOEREN S,PARCY F,XU L,CARLES C C,ANGENENT G C,KAUFMANN K.Characterization of MADSdomain transcription factor complexes in Arabidopsis flower development.Proceedings of the National Academy of Sciences of the USA,2012,109(5):1560-1565.
[16]DEWITTE W,RIOU-KHAMLICHI C,SCOFIELD S,HEALY J,JACQMARD A,KILBY N,MURRAY J.Altered cell cycle distribution,hyperplasia,and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3.Plant Cell,2003,15(1):79-92.
[17]HARADA T,TORII Y,MORITA S,ONODERA R,HARA Y,YOKOYAMA R,NISHITANI K,SATOH S.Cloning,characterization,and expression of xyloglucan endotransglucosylase/hydrolase and expansin genes associated with petal growth and development during carnation flower opening.Journal Of Experimental Botany,2011,62(2):815-823.
[18]YAMAGUCHI N,WU M-F,WINTER C M,BERNS M C,NOLE-WILSON S,YAMAGUCHI A,COUPLAND G,KRIZEK B A,WAGNER D.A molecular framework for auxin-mediated initiation of flower primordia.Developmental Cell,2013,24(3):271-282.
[19]LüP,ZHANG C,LIU J,LIU X,JIANG G,JIANG X,KHAN M A,WANG L,HONG B,GAO J.Rh HB1 mediates the antagonism of gibberellins to ABA and ethylene during rose(Rosa hybrida)petal senescence.The Plant Journal,2014,78(4):578-590.
[20]杨娜,郭维明,陈发棣,房伟民.光周期对秋菊品种’神马’花芽分化和开花的影响.园艺学报,2007,34(4):965-972.YANG N,GUO W M,CHEN F D,FANG W M.Effects of photoperiod on floral bud differentiation and flowering of Chrysanthemum morifolium Ramat.‘Jinba’.Acta Horticulturae Sinica,2007,34(4):965-972.(in Chinese)
[21]JOFUKU K D,DEN BOER B,VAN MONTAGU M,OKAMURO J K.Control of Arabidopsis flower and seed development by the homeotic gene APETALA2.The Plant Cell,1994,6(9):1211-1225.
[22]KRIZEK B A.AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain.Nucleic Acids Research,2003,31(7):1859-1868.
[23]MASAKI T,MITSUI N,TSUKAGOSHI H,NISHII T,MORIKAMI A,NAKAMURA K.ACTIVATOR of Spomin::LUC1/WRINKLED1of Arabidopsis thaliana Transactivates Sugar-inducible Promoters.Plant and Cell Physiology,2005,46(4):547-556.
[24]NOLE-WILSON S,KRIZEK B A.DNA binding properties of the Arabidopsis floral development protein AINTEGUMENTA.Nucleic Acids Research,2000,28(21):4076-4082.
[25]盛慧,秦智伟,李文滨,周秀艳,武涛,辛明.黄瓜生长素反应因子(ARF)家族鉴定及表达特异性分析.中国农业科学,2014,47(10):1985-1994.SHENG H,QIN Z W,LI W B,ZHOU X Y,WU T,XIN M.Genome-wide identification and expression analysis of auxin response factor(ARF)family in cucumber.Scientia Agricultura Sinica,2014,47(10):1985-1994.(in Chinese)
[26]MüLLER B,SHEEN J.Cytokinin and auxin interplay in root stem-cell specification during early embryogenesis.Nature,2008,453(7198):1094-1097.
[27]NOLE-WILSON S,TRANBY T L,KRIZEK B A.AINTEGUMENTAlike(AIL)genes are expressed in young tissues and may specify meristematic or division-competent states.Plant Molecular Biology,2005,57(5):613-628.
[28]MENGES M,SAMLAND A,PLANCHAIS S,MURRAY J.The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis.Plant Cell,2006,18(4):893-906.
[29]RANDALL R,SORNAY E,DEWITTE W,MURRAY J.AINTEGUMENTA and the D-type cyclin CYCD3;1 independently contribute to petal size control in Arabidopsis:evidence for organ size compensation being an emergent rather than a determined property.Journal of Experimental Botany,2015,66(13):3991-4000.
[30]PORCO S,LARRIEU A,DU Y,GAUDINIER A,GOH T,SWARUP K,SWARUP R,KUEMPERS B,BISHOPP A,LAVENUS J,CASIMIRO I,HILL K,BENKOVA E,FUKAKI H,BRADY S,SCHERES B,PéRET B,BENNETT M.Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3.Development,2016,143(18):3340-3349.
[31]GARZA-AGUILAR S,LARA-Nú?EZ A,GARCíA-RAMíREZ E,VáZQUEZ-RAMOS J.Modulation of Cyc D3;1-CDK complexes by phytohormones and sucrose during maize germination.Physiologia Plantarum,2017,160(1):84-97.
[32]VANDENBUSSCHE F,PETRáSEK J,ZáDNíKOVáP,HOYEROVáK,PESEK B,RAZ V,SWARUP R,BENNETT M,ZAZíMALOVáE,BENKOVáE,VAN DER STRAETEN D.The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings.Development,2010,137(4):597-606.
[33]PEAUCELLE A,BRAYBROOK S,LE GUILLOU L,BRON E,KUHLEMEIER C,H?FTE H.Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis.Current Biology,2011,21(20):1720-1726.