小G蛋白ROP6在百脉根结瘤信号途径中功能及作用机制的研究
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摘要
豆科植物分泌类黄酮化合物,能诱导根瘤菌结瘤基因的表达,合成结瘤因子(NF),结瘤因子作为根瘤菌共生信号分子作用于寄主植物,在结瘤起始阶段发挥关键作用。植物中的结瘤因子受体NFR1和NFR5被认为共同参与接收结瘤因子信号,并与之相结合,然后依次将结瘤因子信号传递到下游调控结瘤基因,从而引起宿主植物细胞一系列形态、生理及生化变化。尽管NFR5在百脉根结瘤信号转导中起着至关重要的作用,但是它接收并传递结瘤因子信号的生化机制我们知之甚少。我们用酵母双杂交技术筛选出了与结瘤因子受体NFR5相互作用的蛋白-百脉根小G蛋白ROP6,并证实ROP6作为正调节子参与根瘤菌对豆科植物的侵染和根瘤的发育。其主要研究结果如下：
1.以NFR5激酶结构域(NFR5-PK)为诱饵,通过酵母双杂交系统,筛选百脉根AD-cDNA文库分离得到小GTPase ROP6蛋白。利用体外蛋白pull-down以及烟草体内Co-IP等技术证实了全长的NFR5与ROP6蛋白之间的相互作用。同时构建ROP6的两个突变体,组成型活化突变体ROP6-CA (constitutively active mutants)和功能缺失突变体ROP6-DN (dominant negative mutants)。利用体外蛋白pull-down和烟草体内BiFC实验验证了NFR5与ROP6两个突变体蛋白之间的相互作用。
2.利用基因枪轰击洋葱表皮细胞以及农杆菌介导百脉根毛根转化的方法将ROP6基因导入植物细胞,结果表明ROP6定位于植物细胞的细胞膜和细胞质中。我们用双分子荧光互补技术(BiFC)观察NFR5与ROP6在烟草叶片中的相互作用。ROP6和NFR5分别融合到青色荧光蛋白的N末端(SCN)和C末端(SCC)。SCC:NFR5和ROP6：SCN在烟草叶片细胞中共表达时,在细胞膜观察到强烈的青色荧光信号。BiFC实验证实NFR5与ROP6在植物细胞的细胞膜相互作用。
3.通过薄板层析板(TLC)分离GTP和GDP,放射自显影检测水解产物[a-32P]GDP的方法测定ROP6蛋白的GTPase酶活,结果证实野生型的ROP6能够水解GTP,自身具有微弱的GTP酶活,在反应体系中加入NFR1和/或NFR5蛋白均不影响ROP6的GTPase酶活。
4. Real-time PCR结果显示接种根瘤菌以后ROP6基因在百脉根根中的表达量明显升高。为了从细胞学水平检测ROP6基因的时空表达,我们构建了ROP6Pro:GUS重组质粒,用组织化学染色的方法观察ROP6基因在转化毛根中的表达,结果显示接种根瘤菌之前ROP6在根的维管束,根尖,根毛中均有少量表达,接种之后,这些部位表达量显著增加。并且在发育的根瘤皮层中ROP6基因的表达量较高,而成熟和衰老的根瘤中ROP6的表达量明显降低。启动子实验结果与Real-time PCR结果一致,证实了ROP6基因的表达确实依赖于根瘤菌的侵染。因此我们推测ROP6参与根瘤菌的侵染和根瘤的发育。
5.通过RNA干扰(RNAi)技术下调表达ROP6基因,结果显示ROP6的RNAi抑制了植株侵染线的形成和结瘤的起始,导致RNAi植株结瘤数目明显减少。ROP6RNAi毛根中两个早期结瘤素基因NIN和ENOD40-2的表达受到明显抑制,说明ROP6是早期结瘤素基因诱导表达所必须的。这个结果证实ROP6在共生信号转导途径中发挥正调控作用。
6.利用毛根转化技术将ROP6, ROP6-CA, ROP6-DN导入百脉根中过量表达,观察接种根瘤菌后根毛的变形表型,结果显示过量表达ROP6和ROP6-CA使得根毛的变形增加,而过量表达ROP6-DN使得根毛的变形大大减少。说明ROP6的不同活化状态能够影响根毛对结瘤因子的感知,超表达ROP6和ROP6-CA都能够增强根毛对结瘤因子的感知,而超表达ROP6-DN使得根毛对结瘤因子的感知大大降低。
Production of Nod factor molecule is activated by the release of plant predominantly flavonoids, Nod factors are a novel general class of signal molecules produced by rhizo-bia, which play a key function in the initial steps of nodulation. Both NFR1and NFR5are predicted to participate in the reception and transduction of Nod factor signal, and trans-mit it to the downstream genes. Then, there are a series of physiological and biochemical changes in host plant cells. Although NFR5is known to be essential in the Nod factor signaling in Lotus japonicus, the biochemical mechanism leading to Nod factor-induced transcriptional activation is obscure. In this report we describe a small GTPase ROP6in-teracted with Nod factor receptor NFR5and our experimental data demonstrate a role of ROP6as a positive regulator of infection thread formation and nodulation in L. japonicus. The specific research results are as follows:
1. We use the atypical kinase domain (NFR5-PK) as bait to screen a Lotus cDNA li-brary constructed in the prey vector pGADT7-Rec and identify a small GTPase ROP6. Protein pull-down assay in vitro and Co-IP assay in planta show that the full-length NFR5could interact with ROP6. On the other hand, we construct ROP6-CA (constitutively ac-tive) and ROP6-DN (dominant negative) mutants. Using protein pull down assay in vitro and BiFC assay in planta, we find that NFR5is able to interacte with ROP6-CA and ROP6-DN respectively.
2. ROP6is localized to the plasma membrane and cytoplasm in onion epidermal cells through particle bombardment. Similar localization results are also observed in Lo-tus hairy roots. We perform bimolecular fluorescence complementation (BiFC) to assess the interaction between NFR5and ROP6in tobacco leaves. ROP6and NFR5are fused to the split cyan fluorescent protein N terminus (SCN) and C terminus (SCC), respectively. When SCC:NFR5with ROP6:SCN are coexpressed in the leaf cells, strong cyan fluores-cent signals are detected at the plasma membrane. BiFC assay suggests that ROP6inter-acted with NFR5at the plasma membrane of living plant cells.
3. Purified ROP6is incubated with [a-32P]GTP, and the reaction product [a-32P]GDP is detected by autoradiography on thin-layer chromatography plates (TLC). ROP6is able to hydrolyze GTP to GDP. Only wild-type ROP6has intrinsic GTPase activity without the requirement for NFR1and/or NFR5proteins in vitro.
4. Real-time PCR approach showes that ROP6transcripts are highly expressed in the roots of L. japonicus after inoculation with M. loti. To investigate the spatial pattern of ROP6expression at the cellular level, the ROP6gene promoter is used to drive the ex-pression of the GUS reporter in transgenic hairy roots. Histochemical staining showes that the gene expression is dramatically increased in root vascular bundles, root tips and root hairs after inoculation with M. loti. The activity is concentrated in the cortex of develop-ing nodules and is down-regulated drastically in mature and senescent nodules. These observations are consistent with the results of real-time PCR and confirm that the expres-sion of ROP6gene is indeed dependent on rhizobial infection. These results indicate that ROP6involves in the process of rhizobial infection and nodule development in L. ja-ponicus.
5. Down-regulation of ROP6gene expression by RNA interference (RNAi) signifi-cantly impairs nodulation by inhibiting infection thread formation and nodule initiation. The two nodulation-related marker genes NIN and ENOD40-2transcripts decrease mark-edly in ROP6RNAi hairy roots. These results suggest that ROP6is required for the NF induced expression of early nodulin genes. Thus, ROP6may act as a positive regulator in the process of symbiosis in L. japonicus.
6. Overexpression of ROP6, ROP6-CA and ROP6-DN in L. japonicus lead to differ-ent root hair deformation phenotypes after inoculation with M. loti. Overexpression of ROP6and ROP6-CA increase the root hair deformation, while overexpression of ROP6-DN significantly inhibits the root hair deformation. These results suggest that dif-ferent activation state of ROP6can affect the Nod factor perception of root hairs. Over-expression of ROP6and ROP6-CA can enhance the Nod factor perception, while overex-pression of ROP6-DN greatly reduces the Nod factor perception.
1.以NFR5激酶结构域(NFR5-PK)为诱饵,通过酵母双杂交系统,筛选百脉根AD-cDNA文库分离得到小GTPase ROP6蛋白。利用体外蛋白pull-down以及烟草体内Co-IP等技术证实了全长的NFR5与ROP6蛋白之间的相互作用。同时构建ROP6的两个突变体,组成型活化突变体ROP6-CA (constitutively active mutants)和功能缺失突变体ROP6-DN (dominant negative mutants)。利用体外蛋白pull-down和烟草体内BiFC实验验证了NFR5与ROP6两个突变体蛋白之间的相互作用。
2.利用基因枪轰击洋葱表皮细胞以及农杆菌介导百脉根毛根转化的方法将ROP6基因导入植物细胞,结果表明ROP6定位于植物细胞的细胞膜和细胞质中。我们用双分子荧光互补技术(BiFC)观察NFR5与ROP6在烟草叶片中的相互作用。ROP6和NFR5分别融合到青色荧光蛋白的N末端(SCN)和C末端(SCC)。SCC:NFR5和ROP6：SCN在烟草叶片细胞中共表达时,在细胞膜观察到强烈的青色荧光信号。BiFC实验证实NFR5与ROP6在植物细胞的细胞膜相互作用。
3.通过薄板层析板(TLC)分离GTP和GDP,放射自显影检测水解产物[a-32P]GDP的方法测定ROP6蛋白的GTPase酶活,结果证实野生型的ROP6能够水解GTP,自身具有微弱的GTP酶活,在反应体系中加入NFR1和/或NFR5蛋白均不影响ROP6的GTPase酶活。
4. Real-time PCR结果显示接种根瘤菌以后ROP6基因在百脉根根中的表达量明显升高。为了从细胞学水平检测ROP6基因的时空表达,我们构建了ROP6Pro:GUS重组质粒,用组织化学染色的方法观察ROP6基因在转化毛根中的表达,结果显示接种根瘤菌之前ROP6在根的维管束,根尖,根毛中均有少量表达,接种之后,这些部位表达量显著增加。并且在发育的根瘤皮层中ROP6基因的表达量较高,而成熟和衰老的根瘤中ROP6的表达量明显降低。启动子实验结果与Real-time PCR结果一致,证实了ROP6基因的表达确实依赖于根瘤菌的侵染。因此我们推测ROP6参与根瘤菌的侵染和根瘤的发育。
5.通过RNA干扰(RNAi)技术下调表达ROP6基因,结果显示ROP6的RNAi抑制了植株侵染线的形成和结瘤的起始,导致RNAi植株结瘤数目明显减少。ROP6RNAi毛根中两个早期结瘤素基因NIN和ENOD40-2的表达受到明显抑制,说明ROP6是早期结瘤素基因诱导表达所必须的。这个结果证实ROP6在共生信号转导途径中发挥正调控作用。
6.利用毛根转化技术将ROP6, ROP6-CA, ROP6-DN导入百脉根中过量表达,观察接种根瘤菌后根毛的变形表型,结果显示过量表达ROP6和ROP6-CA使得根毛的变形增加,而过量表达ROP6-DN使得根毛的变形大大减少。说明ROP6的不同活化状态能够影响根毛对结瘤因子的感知,超表达ROP6和ROP6-CA都能够增强根毛对结瘤因子的感知,而超表达ROP6-DN使得根毛对结瘤因子的感知大大降低。
Production of Nod factor molecule is activated by the release of plant predominantly flavonoids, Nod factors are a novel general class of signal molecules produced by rhizo-bia, which play a key function in the initial steps of nodulation. Both NFR1and NFR5are predicted to participate in the reception and transduction of Nod factor signal, and trans-mit it to the downstream genes. Then, there are a series of physiological and biochemical changes in host plant cells. Although NFR5is known to be essential in the Nod factor signaling in Lotus japonicus, the biochemical mechanism leading to Nod factor-induced transcriptional activation is obscure. In this report we describe a small GTPase ROP6in-teracted with Nod factor receptor NFR5and our experimental data demonstrate a role of ROP6as a positive regulator of infection thread formation and nodulation in L. japonicus. The specific research results are as follows:
1. We use the atypical kinase domain (NFR5-PK) as bait to screen a Lotus cDNA li-brary constructed in the prey vector pGADT7-Rec and identify a small GTPase ROP6. Protein pull-down assay in vitro and Co-IP assay in planta show that the full-length NFR5could interact with ROP6. On the other hand, we construct ROP6-CA (constitutively ac-tive) and ROP6-DN (dominant negative) mutants. Using protein pull down assay in vitro and BiFC assay in planta, we find that NFR5is able to interacte with ROP6-CA and ROP6-DN respectively.
2. ROP6is localized to the plasma membrane and cytoplasm in onion epidermal cells through particle bombardment. Similar localization results are also observed in Lo-tus hairy roots. We perform bimolecular fluorescence complementation (BiFC) to assess the interaction between NFR5and ROP6in tobacco leaves. ROP6and NFR5are fused to the split cyan fluorescent protein N terminus (SCN) and C terminus (SCC), respectively. When SCC:NFR5with ROP6:SCN are coexpressed in the leaf cells, strong cyan fluores-cent signals are detected at the plasma membrane. BiFC assay suggests that ROP6inter-acted with NFR5at the plasma membrane of living plant cells.
3. Purified ROP6is incubated with [a-32P]GTP, and the reaction product [a-32P]GDP is detected by autoradiography on thin-layer chromatography plates (TLC). ROP6is able to hydrolyze GTP to GDP. Only wild-type ROP6has intrinsic GTPase activity without the requirement for NFR1and/or NFR5proteins in vitro.
4. Real-time PCR approach showes that ROP6transcripts are highly expressed in the roots of L. japonicus after inoculation with M. loti. To investigate the spatial pattern of ROP6expression at the cellular level, the ROP6gene promoter is used to drive the ex-pression of the GUS reporter in transgenic hairy roots. Histochemical staining showes that the gene expression is dramatically increased in root vascular bundles, root tips and root hairs after inoculation with M. loti. The activity is concentrated in the cortex of develop-ing nodules and is down-regulated drastically in mature and senescent nodules. These observations are consistent with the results of real-time PCR and confirm that the expres-sion of ROP6gene is indeed dependent on rhizobial infection. These results indicate that ROP6involves in the process of rhizobial infection and nodule development in L. ja-ponicus.
5. Down-regulation of ROP6gene expression by RNA interference (RNAi) signifi-cantly impairs nodulation by inhibiting infection thread formation and nodule initiation. The two nodulation-related marker genes NIN and ENOD40-2transcripts decrease mark-edly in ROP6RNAi hairy roots. These results suggest that ROP6is required for the NF induced expression of early nodulin genes. Thus, ROP6may act as a positive regulator in the process of symbiosis in L. japonicus.
6. Overexpression of ROP6, ROP6-CA and ROP6-DN in L. japonicus lead to differ-ent root hair deformation phenotypes after inoculation with M. loti. Overexpression of ROP6and ROP6-CA increase the root hair deformation, while overexpression of ROP6-DN significantly inhibits the root hair deformation. These results suggest that dif-ferent activation state of ROP6can affect the Nod factor perception of root hairs. Over-expression of ROP6and ROP6-CA can enhance the Nod factor perception, while overex-pression of ROP6-DN greatly reduces the Nod factor perception.
引文
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