拟南芥生长素糖基转移酶基因UGT74D1的鉴定及功能研究
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摘要
生长素作为植物的一种重要内源激素,参与调控植物生长发育的诸多过程,如根、茎、叶的发育、维管束组织的形成和分化、植物的向地和向光反应、器官的衰老等。植物体内生长素含量的动态平衡与植物的生长发育、环境应答等有密切的关系。长期以来,虽然对生长素在遗传学、生物化学以及生理学等方面进行了大量研究,但对生长素糖基化修饰及其生理学意义的认识仍然有限。生长素的糖基化修饰主要发生在吲哚环侧链的羧基上,并且主要是添加葡萄糖。目前,糖基化修饰被认为是调控植物活性激素在不同组织细胞中动态平衡的重要机制之一,是对生长素进行精细调控的重要手段,这种调控与植物的生理状态、发育阶段、环境条件、生物和非生物胁迫等因素密切相关,对植物维持的正常生长发育起重要作用。
糖基转移酶是专门负责催化分子的糖基化修饰反应的酶类,它将活性糖基从供体(通常是尿嘧啶核苷二磷酸-葡萄糖UDP-glucose)转移到激素、次级代谢物、病原菌侵染物以及植物内外源毒性物质等一系列植物小分子化合物受体上。被糖基化修饰后的植物小分子往往会改变它们的生物活性、水溶性、稳定性、在细胞内和整体植株中的运输特性、亚细胞定位以及与受体的相互识别与结合特性。另外还能降低或消除内源和外源物质的毒性。因此,糖基化修饰在调节包括植物激素活性在内的细胞代谢平衡、维持植物正常生长发育等方面有重要意义
本论文选题来自于国家自然基金课题,总的思路是以体外生化实验为基础,对拟南芥糖基转移酶家族1进行了生长素糖基转移酶活性的筛选,鉴定到生长素的特异糖基转移酶基因UGT74D1,研究这个糖基转移酶的相关生化特征。接着转向体内遗传实验,以拟南芥为实验材料,分析生长素糖基转移酶基因UGT74D1在植物体内所起的作用,确定它们在体内的生长素糖基化修饰功能,从而为深入了解生长素糖基化的分子基础及其功能基因表达的生理学意义提供依据。本论文主要的研究内容及结果如下：
1.原核系统表达多个糖基转移酶候选基因,通过生化方法鉴定了一个新的生长素糖基转移酶UGT74D1.
将多个候选基因转到pGEX系统的原核表达载体上,在大肠杆菌XL1-Blue中表达并得到了纯化的酶蛋白。用纯化出的候选基因融合蛋白分别与多种生长素及其结构类似物进行酶促反应,反应产物经过HPLC和LC-MS鉴定,鉴定了一个新的生长素糖基转移酶UGT74D1,发现该酶能够高效地糖基化修饰IBA、 IAA等天然的植物生长素。
2.研究了糖基转移酶UGT74D1的酶学性质。
相同的实验条件下,对比UGT74D1对6种生长素及其结构类似物的相对转化率,确定了该酶在体外的最适催化底物为IBA。以底物IBA为例,研究了温度对酶活性的影响,发现37℃时活性最高；研究了各种缓冲液及pH对酶活性的影响,发现在HEPES缓冲液,pH=6.0时活性最高。刚时对IBA进行了酶学动力学分析。
3.确定了生长素糖基转移酶基因UGT74D1的表达模式以及编码产物的亚细胞定位。
GUS组织化学染色实验表明,在1-7天之内的幼苗期,UGT74D1在子叶下胚轴与根的连接处、根尖中都有较强表达。在随后的生长发育阶段8-14天,UGT74D1在新生的真叶、真叶叶脉中、主根根尖、侧根有很强的农达。随后生长发育期35天时,花序、幼嫩角果皮、茎叶的叶脉、根中都有较强的表达。尤其随着真叶的成熟,UGT74D1的表达逐渐由叶片中心向叶片边缘处集中,推断其时空组织特异性表达变化导致了过农达体莲卒叶发生了卷曲表型。
通过基因枪转化洋葱表皮细胞,观察了融合基因的瞬间表达情况。在扫描激光共聚焦显微镜下观察,发现生长索糖基转移酶UGT74D1定位在细胞质和细胞核中。说明此生长素糖基转移酶在整个细胞中都发挥糖基化修饰作用。
4.糖基转移酶UGT74D1在植物体内能够使生长素发生糖基化修饰,参与调控植物对生长素的响应,影响植物的生长发育。
提取了不同株系的植物蛋白,对生长素进行酶促反应,发现过表达株系的植物蛋白对生长素的糖基化修饰活性明显高于野生型和双突变体。测定了外源IBA处理下不同基因型植株体内IBA-糖酯含量,发现双突变体中IBA-糖酯含量的增幅显著降低,而过表达体中IBA-糖酯含量的增幅明显升高,从而证明UGT74D1基因在植物体内能糖基化修饰生长素。
利用野生型拟南芥Col-0、UGT74D1T-DNA插入突变体、UGT74Dl UGT74E2双突变纯合体和UGT74D1基因过表达体为材料,通过添加不同浓度的外源生长素IBA或IAA,比较了它们在主根延伸抑制、侧根密度等方面的差异。实验表明,突变体对外源添加的生长素较野生型敏感,而过表达体较野生型不敏感。UGT74D1过表达株系与DR5::GUS转基因株系杂交后,GUS染色结果表明其对生长素的响应明显比对照组减弱。说明了UGT74D1能够通过糖基化修饰使生长素失活,影响植物对生长素的响应。
在正常生长条件下,UGT74D1过表达植株表现出叶子发生卷曲,并且叶柄夹角变小。表明UGT74D1在植物体内有重要的生理学作用,能够影响植物的生长发育。
总之,本论文首次在拟南芥中鉴定出UGT74D1是生长素糖基转移酶,并用遗传学方法证明糖基转移酶UGT74D1在植物体内能够使生长素发生糖基化修饰,参与调控植物对生长素的响应,影响植物的生长发育。这些结果为进一步研究生长素的代谢调节及深入理解生长素发挥作用的分子机理奠定了基础,具有重要理论意义。
Auxin is one type of phytohormones that plays important roles in nearly all aspects of plant growth and developmental processes, such as the development of root, shoot and leaf, vascular initiation and differentiation, geotropism and phototropism, organic senescence etc. The homeostasis of endogenous auxins is the maintenance of a steady state concentration of the auxins in the receptive tissue appropriate to any fixed environmental condition. Since their discovery, although numerous work have been done to study the auxins' physiological function during plant growth and development by genetics, biochemistry and physiology, the significance of their modification by glycosylation is still largely unknown. Glycoslation of auxins takes place on the carboxyl group of the side chain of indole ring, and usually uses UDP-Glc as activated sugar donor. Glycosylation is the most universal modification in plant and it is thought to be one of most important mechanisms to precisely control auxin homeostasis for plant in order to keep normal growth and development under different developmental stage and various environments.
Glycosyltransferases can typically transfer single or multiple activated sugars from a donor (usually nucleotide sugar UDP-glucose) to a wide range of small molecular acceptors including hormones, secondary metabolites and abiotic chemicals and toxins from the environment. Glycosylation modification will often change the plant molecules in their biological activity, water-solubility, stability, transport characteristics, subcellular localization and binding properties with receptors, and also can reduce or eliminate the toxicity of endogenous and exogenous substances. Therefore, glycosylation plays a key role in maintaining cell homeostasis, thus likely participating in the regulation of plant growth and development.
This research project was supported by grants from the National Natural Science Foundation of China. In this study, the in vitro biochemical screening of the group L of Arabidopsis thaliana glycosyltransferase superfamily was firstly carried out for the enzymatic activity toward auxins. UGT74D1was identified to be a novel auxin glycosyltransferase. Next, the physiological role of auxin glucosyltransferase UGT74D1in planta was investigated through a molecular genetic approach. Our data obtained from this study provide an important reference for further understanding of the auxin regulation by glycosylation in plants.
The main contents and results of this study are as follows:
1. Several candidate glycosyltransferases were expressed using prokaryotic system and UGT74D1was identified to be a novel auxin glycosyltransferase.
Candidate genes were constructed to pGEX prokaryotic expression vectors, expressed in E.coli XL1-Blue, and then recombinant proteins were purified. The enzyme activities of the recombinant proteins were analyzed by incubating them separately with7auxins and analogs used as substrates. Following HPLC and LC-MS analyses of the reaction products, it was found that the recombinant UGT74D1had a strong activity toward natural auxins IBA and IAA.
2. The enzymatic properties of glycosyltranferase UGT74D1were studied.
Under the same condition, relative conversion rates of these7auxin substrates were calculated and it was found that UGT74D1had a highest enzymatic activity toward IBA in vitro. Taking IBA as an example, the influence factors of enzymatic activity including temperature, pH were tested. The results showed that37centigrade degree was the best temperature for maximum enzyme activity. The pH optimum was HEPES buffer with pH6.0. Enzyme kinetic parameters of UGT74D1toward IBA were also investigated.
3. The expression pattern and subcellular localization of UGT74D1were analyzed.
UGT74D1promoter::GUS reporter construct was introduced into Arabidosis and GUS histochemical assay was used for UGT74D1expression pattern analysis. UGT74D1was intensively expressed in cotyledons, hypocotyl-root junction and primary root tip for the first7days of seedlings. UGT74D1was also expressed in young leaves, leaf vein, primary root tip and lateral roots for the one to two week old seedlings. For the5-week-old seedlings, UGT74D1was highly expressed in inflorescences, young silique capsule, cauline leaf vein and root. Insterestly, the UGT74D1expression was observed to concentrate at the marginal region of developed leaves.
Green fluorescent protein fusion vector of UGT74D1was introduced into onion epidermal cells by particle bombardment technology. The observation of green fluorescence showed that the auxins glycosyltransferase UGT74D1was localized in cytoplasm and nucleus, indicating its subcellular action sites.
4. UGT74D1can glucosylate auxins in planta, thus regulate plant response to auxins and impact on the plant growth and development.
In order to know the physiological role of UGT74D1, all the T-DNA mutant (ugt74d1), double mutant (ugt74dlugt74e2) and overexpression lines (UGT74D1OEs) were obtained. Crude protein extracts from seedlings of different lines were analyzed for enzyme activity toward auxins. The results showed that lines with higher UGT74D1transcripts also displayed stronger enzyme activity toward tested auxins to form their glucose conjugates. When exogenous IBA was applied to different plant lines, much higher level of IBA-glucose in overexpression lines than in mutants and wild type plants can be observed. These data indicated that over-production of the UGT74D1in the plants indeed led to increased level of the glucose conjugate of IBA, suggesting an in vivo glucosylating role of UGT74D1to plant auxins.
Plant response to auxins was investigated by measuring root elongation and lateral root density under the application of exogenous auxins IBA and IAA to different lines described above. Mutants showed a more sensitive phenotype both in root elongation and lateral root density than wild type. In contrast, overexpression lines were relatively insensitive than wild type, suggesting that UGT74D1regulated plant responses to auxins possibly by deactivating auxins. Furthermore, we employed the pDR5:GUS reporter construct to explore the possible role of UGT74D1in auxin signaling. It was found that auxin signaling was much reduced in UGT74D1overexpression lines than in wild type plants, indicating that UGT74D1might regulate the auxin signaling through glucosylating and thus deactivating auxin approach.
More interesting finding in this study is the changes in plant phenotype. Under normal growth conditions, it was found that UGT74D1overexpression lines displayed less erect petioles and curling leaves. These phenotypic changes were well maintained under different light intensity. These findings implicated that UGT74D1had an important physiological role in modulating plant growth and development.
In summary, a novel auxin glucosyltransferase, UGT74D1, was biochemically identified from Arabidopsis in this study. Further, the auxin glucosylating activiyt of glucosyltransferase UGT74D1in planta was demonstrated through a molecular genetic approach. Moreover, the physiological role of UGT74D1was found in regulating auxin response and modulating plant growth and development. All these results provide theoretical basis for a better understanding of molecular mechanisms of auxin glucosylation and auxin regulation in planta.
糖基转移酶是专门负责催化分子的糖基化修饰反应的酶类,它将活性糖基从供体(通常是尿嘧啶核苷二磷酸-葡萄糖UDP-glucose)转移到激素、次级代谢物、病原菌侵染物以及植物内外源毒性物质等一系列植物小分子化合物受体上。被糖基化修饰后的植物小分子往往会改变它们的生物活性、水溶性、稳定性、在细胞内和整体植株中的运输特性、亚细胞定位以及与受体的相互识别与结合特性。另外还能降低或消除内源和外源物质的毒性。因此,糖基化修饰在调节包括植物激素活性在内的细胞代谢平衡、维持植物正常生长发育等方面有重要意义
本论文选题来自于国家自然基金课题,总的思路是以体外生化实验为基础,对拟南芥糖基转移酶家族1进行了生长素糖基转移酶活性的筛选,鉴定到生长素的特异糖基转移酶基因UGT74D1,研究这个糖基转移酶的相关生化特征。接着转向体内遗传实验,以拟南芥为实验材料,分析生长素糖基转移酶基因UGT74D1在植物体内所起的作用,确定它们在体内的生长素糖基化修饰功能,从而为深入了解生长素糖基化的分子基础及其功能基因表达的生理学意义提供依据。本论文主要的研究内容及结果如下：
1.原核系统表达多个糖基转移酶候选基因,通过生化方法鉴定了一个新的生长素糖基转移酶UGT74D1.
将多个候选基因转到pGEX系统的原核表达载体上,在大肠杆菌XL1-Blue中表达并得到了纯化的酶蛋白。用纯化出的候选基因融合蛋白分别与多种生长素及其结构类似物进行酶促反应,反应产物经过HPLC和LC-MS鉴定,鉴定了一个新的生长素糖基转移酶UGT74D1,发现该酶能够高效地糖基化修饰IBA、 IAA等天然的植物生长素。
2.研究了糖基转移酶UGT74D1的酶学性质。
相同的实验条件下,对比UGT74D1对6种生长素及其结构类似物的相对转化率,确定了该酶在体外的最适催化底物为IBA。以底物IBA为例,研究了温度对酶活性的影响,发现37℃时活性最高；研究了各种缓冲液及pH对酶活性的影响,发现在HEPES缓冲液,pH=6.0时活性最高。刚时对IBA进行了酶学动力学分析。
3.确定了生长素糖基转移酶基因UGT74D1的表达模式以及编码产物的亚细胞定位。
GUS组织化学染色实验表明,在1-7天之内的幼苗期,UGT74D1在子叶下胚轴与根的连接处、根尖中都有较强表达。在随后的生长发育阶段8-14天,UGT74D1在新生的真叶、真叶叶脉中、主根根尖、侧根有很强的农达。随后生长发育期35天时,花序、幼嫩角果皮、茎叶的叶脉、根中都有较强的表达。尤其随着真叶的成熟,UGT74D1的表达逐渐由叶片中心向叶片边缘处集中,推断其时空组织特异性表达变化导致了过农达体莲卒叶发生了卷曲表型。
通过基因枪转化洋葱表皮细胞,观察了融合基因的瞬间表达情况。在扫描激光共聚焦显微镜下观察,发现生长索糖基转移酶UGT74D1定位在细胞质和细胞核中。说明此生长素糖基转移酶在整个细胞中都发挥糖基化修饰作用。
4.糖基转移酶UGT74D1在植物体内能够使生长素发生糖基化修饰,参与调控植物对生长素的响应,影响植物的生长发育。
提取了不同株系的植物蛋白,对生长素进行酶促反应,发现过表达株系的植物蛋白对生长素的糖基化修饰活性明显高于野生型和双突变体。测定了外源IBA处理下不同基因型植株体内IBA-糖酯含量,发现双突变体中IBA-糖酯含量的增幅显著降低,而过表达体中IBA-糖酯含量的增幅明显升高,从而证明UGT74D1基因在植物体内能糖基化修饰生长素。
利用野生型拟南芥Col-0、UGT74D1T-DNA插入突变体、UGT74Dl UGT74E2双突变纯合体和UGT74D1基因过表达体为材料,通过添加不同浓度的外源生长素IBA或IAA,比较了它们在主根延伸抑制、侧根密度等方面的差异。实验表明,突变体对外源添加的生长素较野生型敏感,而过表达体较野生型不敏感。UGT74D1过表达株系与DR5::GUS转基因株系杂交后,GUS染色结果表明其对生长素的响应明显比对照组减弱。说明了UGT74D1能够通过糖基化修饰使生长素失活,影响植物对生长素的响应。
在正常生长条件下,UGT74D1过表达植株表现出叶子发生卷曲,并且叶柄夹角变小。表明UGT74D1在植物体内有重要的生理学作用,能够影响植物的生长发育。
总之,本论文首次在拟南芥中鉴定出UGT74D1是生长素糖基转移酶,并用遗传学方法证明糖基转移酶UGT74D1在植物体内能够使生长素发生糖基化修饰,参与调控植物对生长素的响应,影响植物的生长发育。这些结果为进一步研究生长素的代谢调节及深入理解生长素发挥作用的分子机理奠定了基础,具有重要理论意义。
Auxin is one type of phytohormones that plays important roles in nearly all aspects of plant growth and developmental processes, such as the development of root, shoot and leaf, vascular initiation and differentiation, geotropism and phototropism, organic senescence etc. The homeostasis of endogenous auxins is the maintenance of a steady state concentration of the auxins in the receptive tissue appropriate to any fixed environmental condition. Since their discovery, although numerous work have been done to study the auxins' physiological function during plant growth and development by genetics, biochemistry and physiology, the significance of their modification by glycosylation is still largely unknown. Glycoslation of auxins takes place on the carboxyl group of the side chain of indole ring, and usually uses UDP-Glc as activated sugar donor. Glycosylation is the most universal modification in plant and it is thought to be one of most important mechanisms to precisely control auxin homeostasis for plant in order to keep normal growth and development under different developmental stage and various environments.
Glycosyltransferases can typically transfer single or multiple activated sugars from a donor (usually nucleotide sugar UDP-glucose) to a wide range of small molecular acceptors including hormones, secondary metabolites and abiotic chemicals and toxins from the environment. Glycosylation modification will often change the plant molecules in their biological activity, water-solubility, stability, transport characteristics, subcellular localization and binding properties with receptors, and also can reduce or eliminate the toxicity of endogenous and exogenous substances. Therefore, glycosylation plays a key role in maintaining cell homeostasis, thus likely participating in the regulation of plant growth and development.
This research project was supported by grants from the National Natural Science Foundation of China. In this study, the in vitro biochemical screening of the group L of Arabidopsis thaliana glycosyltransferase superfamily was firstly carried out for the enzymatic activity toward auxins. UGT74D1was identified to be a novel auxin glycosyltransferase. Next, the physiological role of auxin glucosyltransferase UGT74D1in planta was investigated through a molecular genetic approach. Our data obtained from this study provide an important reference for further understanding of the auxin regulation by glycosylation in plants.
The main contents and results of this study are as follows:
1. Several candidate glycosyltransferases were expressed using prokaryotic system and UGT74D1was identified to be a novel auxin glycosyltransferase.
Candidate genes were constructed to pGEX prokaryotic expression vectors, expressed in E.coli XL1-Blue, and then recombinant proteins were purified. The enzyme activities of the recombinant proteins were analyzed by incubating them separately with7auxins and analogs used as substrates. Following HPLC and LC-MS analyses of the reaction products, it was found that the recombinant UGT74D1had a strong activity toward natural auxins IBA and IAA.
2. The enzymatic properties of glycosyltranferase UGT74D1were studied.
Under the same condition, relative conversion rates of these7auxin substrates were calculated and it was found that UGT74D1had a highest enzymatic activity toward IBA in vitro. Taking IBA as an example, the influence factors of enzymatic activity including temperature, pH were tested. The results showed that37centigrade degree was the best temperature for maximum enzyme activity. The pH optimum was HEPES buffer with pH6.0. Enzyme kinetic parameters of UGT74D1toward IBA were also investigated.
3. The expression pattern and subcellular localization of UGT74D1were analyzed.
UGT74D1promoter::GUS reporter construct was introduced into Arabidosis and GUS histochemical assay was used for UGT74D1expression pattern analysis. UGT74D1was intensively expressed in cotyledons, hypocotyl-root junction and primary root tip for the first7days of seedlings. UGT74D1was also expressed in young leaves, leaf vein, primary root tip and lateral roots for the one to two week old seedlings. For the5-week-old seedlings, UGT74D1was highly expressed in inflorescences, young silique capsule, cauline leaf vein and root. Insterestly, the UGT74D1expression was observed to concentrate at the marginal region of developed leaves.
Green fluorescent protein fusion vector of UGT74D1was introduced into onion epidermal cells by particle bombardment technology. The observation of green fluorescence showed that the auxins glycosyltransferase UGT74D1was localized in cytoplasm and nucleus, indicating its subcellular action sites.
4. UGT74D1can glucosylate auxins in planta, thus regulate plant response to auxins and impact on the plant growth and development.
In order to know the physiological role of UGT74D1, all the T-DNA mutant (ugt74d1), double mutant (ugt74dlugt74e2) and overexpression lines (UGT74D1OEs) were obtained. Crude protein extracts from seedlings of different lines were analyzed for enzyme activity toward auxins. The results showed that lines with higher UGT74D1transcripts also displayed stronger enzyme activity toward tested auxins to form their glucose conjugates. When exogenous IBA was applied to different plant lines, much higher level of IBA-glucose in overexpression lines than in mutants and wild type plants can be observed. These data indicated that over-production of the UGT74D1in the plants indeed led to increased level of the glucose conjugate of IBA, suggesting an in vivo glucosylating role of UGT74D1to plant auxins.
Plant response to auxins was investigated by measuring root elongation and lateral root density under the application of exogenous auxins IBA and IAA to different lines described above. Mutants showed a more sensitive phenotype both in root elongation and lateral root density than wild type. In contrast, overexpression lines were relatively insensitive than wild type, suggesting that UGT74D1regulated plant responses to auxins possibly by deactivating auxins. Furthermore, we employed the pDR5:GUS reporter construct to explore the possible role of UGT74D1in auxin signaling. It was found that auxin signaling was much reduced in UGT74D1overexpression lines than in wild type plants, indicating that UGT74D1might regulate the auxin signaling through glucosylating and thus deactivating auxin approach.
More interesting finding in this study is the changes in plant phenotype. Under normal growth conditions, it was found that UGT74D1overexpression lines displayed less erect petioles and curling leaves. These phenotypic changes were well maintained under different light intensity. These findings implicated that UGT74D1had an important physiological role in modulating plant growth and development.
In summary, a novel auxin glucosyltransferase, UGT74D1, was biochemically identified from Arabidopsis in this study. Further, the auxin glucosylating activiyt of glucosyltransferase UGT74D1in planta was demonstrated through a molecular genetic approach. Moreover, the physiological role of UGT74D1was found in regulating auxin response and modulating plant growth and development. All these results provide theoretical basis for a better understanding of molecular mechanisms of auxin glucosylation and auxin regulation in planta.
引文
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