水稻SINA泛素连接酶OsDIS1的功能分析和作用机制研究
摘要
逆境胁迫严重影响农作物的产量和质量,制约着全球的农业生产,是人口日益增长情况下实现农业可持续发展的重大挑战。泛素介导的蛋白酶体途径是植物体内蛋白质修饰最重要的调控机制之一,其功能涉及植物细胞周期和光周期调控、激素信号转导、新陈代谢调控和DNA修复等多个过程,研究表明泛素介导的蛋白酶体途径也参与对生物胁迫和非生物胁迫的调控。本论文通过生物化学、分子生物学和遗传学相结合的方法对SINA泛素连接酶OsDIS1蛋白的生化功能和参与的生物学过程进行了全面的阐述,并对OsDIS1的作用机制进行了深入的探讨。
体外泛素化反应表明OsDIS1蛋白具有时间依赖的泛素化活性并且C3HC4类型RING finger结构域的完整对其E3泛素连接酶活性是必须的。烟草注射和水稻原生质体转染显示OsDIS1主要定位在细胞核中,同时在细胞膜和细胞质中有些许分布。我们通过过表达和RNAi干扰两种方法构建转基因株系对其生物学功能进行研究,干旱处理结果表明OsDIS1过量表达削弱了水稻对干旱的抗耐性,而RNAi干扰抑制表达却增强了水稻对干旱的抗耐性。为了研究OsDIS1参与干旱胁迫调控的作用机制,我们对OsDIS1过表达植物和对照植物在干旱处理前后进行了全基因组表达分析,发现OsDIS1基因在转录水平上主要通过抑制一系列干旱正调控因子和诱导一系列干旱负调控因子的表达而负调控水稻的干旱胁迫响应过程。我们同时利用酵母双杂交方法筛选OsDIS1的相互作用蛋白,并通过体外GST pull-down和体内免疫共沉淀等方法验证,发现OsDIS1与一个丝氨酸/苏氨酸类激酶OsNek6(?)互作用。亚细胞共定位显示OsDIS1与OsNek6不能共存,但是OsDIS1缺少泛素连接酶活性的突变蛋白OsDIS1(H71Y)却可以和OsNek6有很好的共定位,进一步OsNek6体内降解实验显示OsDIS1可促进OsNek6在体内的降解,而其突变蛋白OsDIS1(H71Y)丧失了这种活性。MG132处理结果显示OsNek6是通过依赖于泛素/26S蛋白酶体的途径降解的,结合体内降解实验,我们认为OsDIS1可通过泛素化促进OsNek6的降解,OsNek6可能是OsDIS1泛素化的底物。酵母双杂交同时验证OsDIS1与一个干旱正调节子OsSKIPa相互作用,并通过体内免疫共沉淀证实。虽然MG132处理结果显示OsSKIPa也是通过依赖于泛素/26S蛋白酶体的途径降解的,但OsSKIPa体内降解试验以及其在OsDIS1转基因水稻中的表达表明在这两种条件下,OsDIS1并不能促进OsSKIPa蛋白的降解。以上结果表明,OsDIS1在转录水平上通过调节一系列逆境相关基因的表达,翻译后修饰水平上通过和OsNek6以及OsSKIPa互作调控水稻的干旱胁迫响应过程。
Stresses seriously affect crop yields and quality, and constrain the global agricultural production, which has become the main challenges for sustainable development of agriculture with the growing population. Ubiquitin-protease pathway (UPS) is one of the most important regulation mechanisms for protein modification in plants. It functions in cell cycle and light cycle regulation, hormone signal transduction, metabolic regulation, DNA repair and responses to biotic and abiotic stresses. In this study, by combining biochemistry, plant molecular biology and genetics methods, we characterized the biological and biochemical functions of the SINA E3ubiquitin ligase OsDIS1(O. sativa drought induced SINA protein1) and elucidated the relationship with its interacting proteins in rice.
In vitro ubiquitination assays showed that OsDIS1possessed time-dependent E3ubiquitin ligase activity, and that the RING finger conserved region was required for the activity. Nicotiana benthamiana transient expression assays and rice protoplast transfection indicated that OsDIS1was localized predominantly in the nucleus, as well as some localized in the cytoplasm and cytomembrane. Both OsDIS1overexpresson and RNAi transgenic lines were produced. Drought treatments showed that overexpression of OsDIS1reduced drought tolerance in transgenic rice plants while RNAi silencing of OsDIS1enhanced drought tolerance. Microarray analysis revealed that many drought responsive genes were induced or suppressed in the OsDIS1overexpression plants under normal and drought conditions. Yeast two-hybrid (Y2H) screening showed that OsDIS1interacted with OsNek6, a serine/threonine protein kinase and the interaction was confirmed by GST pull-down and in vivo co-immunoprecipitation assays. Co-sublocalization of OsDIS1and OsNek6showed that OsDIS1was not able to coexist with OsNek6while the mutant OsDIS1(H71Y) did. OsNek6in vivo degradation assay demonstrated that OsDIS1promoted OsNek6degradation while the OsDIS1(H71Y) mutant did not. The MG132treatment showed that OsNek6was degraded via the26S proteosome-dependent pathway. It seems that OsNek6degradtion via OsDIS1-mediated ubiquitination and OsNek6is the substrate of OsDIS1in rice.Y2H assays also showed that OsDIS1interacted with the drought positive regulator OsSKIPa, which was confirmed by in vivo co-immunoprecipitation assays. The in vivo degradation and expression assays in the OsDISl overexpression and RNAi transgenic plants revealed that OsDIS1was not able to promote OsSKIPa protein degradation in rice. Together, these results demonstrate that OsDIS1plays a negative role in drought stress responses through transcriptional regulation of diverse stress-related genes and post-translational regulation of OsNek6and OsSKIPa in rice.
体外泛素化反应表明OsDIS1蛋白具有时间依赖的泛素化活性并且C3HC4类型RING finger结构域的完整对其E3泛素连接酶活性是必须的。烟草注射和水稻原生质体转染显示OsDIS1主要定位在细胞核中,同时在细胞膜和细胞质中有些许分布。我们通过过表达和RNAi干扰两种方法构建转基因株系对其生物学功能进行研究,干旱处理结果表明OsDIS1过量表达削弱了水稻对干旱的抗耐性,而RNAi干扰抑制表达却增强了水稻对干旱的抗耐性。为了研究OsDIS1参与干旱胁迫调控的作用机制,我们对OsDIS1过表达植物和对照植物在干旱处理前后进行了全基因组表达分析,发现OsDIS1基因在转录水平上主要通过抑制一系列干旱正调控因子和诱导一系列干旱负调控因子的表达而负调控水稻的干旱胁迫响应过程。我们同时利用酵母双杂交方法筛选OsDIS1的相互作用蛋白,并通过体外GST pull-down和体内免疫共沉淀等方法验证,发现OsDIS1与一个丝氨酸/苏氨酸类激酶OsNek6(?)互作用。亚细胞共定位显示OsDIS1与OsNek6不能共存,但是OsDIS1缺少泛素连接酶活性的突变蛋白OsDIS1(H71Y)却可以和OsNek6有很好的共定位,进一步OsNek6体内降解实验显示OsDIS1可促进OsNek6在体内的降解,而其突变蛋白OsDIS1(H71Y)丧失了这种活性。MG132处理结果显示OsNek6是通过依赖于泛素/26S蛋白酶体的途径降解的,结合体内降解实验,我们认为OsDIS1可通过泛素化促进OsNek6的降解,OsNek6可能是OsDIS1泛素化的底物。酵母双杂交同时验证OsDIS1与一个干旱正调节子OsSKIPa相互作用,并通过体内免疫共沉淀证实。虽然MG132处理结果显示OsSKIPa也是通过依赖于泛素/26S蛋白酶体的途径降解的,但OsSKIPa体内降解试验以及其在OsDIS1转基因水稻中的表达表明在这两种条件下,OsDIS1并不能促进OsSKIPa蛋白的降解。以上结果表明,OsDIS1在转录水平上通过调节一系列逆境相关基因的表达,翻译后修饰水平上通过和OsNek6以及OsSKIPa互作调控水稻的干旱胁迫响应过程。
Stresses seriously affect crop yields and quality, and constrain the global agricultural production, which has become the main challenges for sustainable development of agriculture with the growing population. Ubiquitin-protease pathway (UPS) is one of the most important regulation mechanisms for protein modification in plants. It functions in cell cycle and light cycle regulation, hormone signal transduction, metabolic regulation, DNA repair and responses to biotic and abiotic stresses. In this study, by combining biochemistry, plant molecular biology and genetics methods, we characterized the biological and biochemical functions of the SINA E3ubiquitin ligase OsDIS1(O. sativa drought induced SINA protein1) and elucidated the relationship with its interacting proteins in rice.
In vitro ubiquitination assays showed that OsDIS1possessed time-dependent E3ubiquitin ligase activity, and that the RING finger conserved region was required for the activity. Nicotiana benthamiana transient expression assays and rice protoplast transfection indicated that OsDIS1was localized predominantly in the nucleus, as well as some localized in the cytoplasm and cytomembrane. Both OsDIS1overexpresson and RNAi transgenic lines were produced. Drought treatments showed that overexpression of OsDIS1reduced drought tolerance in transgenic rice plants while RNAi silencing of OsDIS1enhanced drought tolerance. Microarray analysis revealed that many drought responsive genes were induced or suppressed in the OsDIS1overexpression plants under normal and drought conditions. Yeast two-hybrid (Y2H) screening showed that OsDIS1interacted with OsNek6, a serine/threonine protein kinase and the interaction was confirmed by GST pull-down and in vivo co-immunoprecipitation assays. Co-sublocalization of OsDIS1and OsNek6showed that OsDIS1was not able to coexist with OsNek6while the mutant OsDIS1(H71Y) did. OsNek6in vivo degradation assay demonstrated that OsDIS1promoted OsNek6degradation while the OsDIS1(H71Y) mutant did not. The MG132treatment showed that OsNek6was degraded via the26S proteosome-dependent pathway. It seems that OsNek6degradtion via OsDIS1-mediated ubiquitination and OsNek6is the substrate of OsDIS1in rice.Y2H assays also showed that OsDIS1interacted with the drought positive regulator OsSKIPa, which was confirmed by in vivo co-immunoprecipitation assays. The in vivo degradation and expression assays in the OsDISl overexpression and RNAi transgenic plants revealed that OsDIS1was not able to promote OsSKIPa protein degradation in rice. Together, these results demonstrate that OsDIS1plays a negative role in drought stress responses through transcriptional regulation of diverse stress-related genes and post-translational regulation of OsNek6and OsSKIPa in rice.
引文
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