摘要
豆科植物与根瘤菌之间的根瘤共生(RNS, root nodule symbiosis)固氮系统是自然界中氮素最有效和经济的来源,在农业与生态学方面具有十分重要的意义。共生体根瘤的形成是紧密协调调控根瘤菌侵染和根瘤器官发生的一个过程,同时伴随一系列的信号转导,其中最重要的就是结瘤因子信号转导。近十年来,以模式豆科植物苜蓿(Medicago truncatula)和百脉根(Lotus japonicus)为材料,在宿主植物中鉴定出一系列与结瘤因子信号转导相关的基因,初步建立了共生信号转导模式图。其中百脉根共生受体样激酶(symbiosis receptor-like kinase, SymRK)是结瘤因子信号转导途径中很重要的一个组分,决定了根瘤菌能否进入植物体内。但是关于它是怎样接收细菌信号以及如何把信号传递下去,目前知之甚少。本研究通过酵母双杂交技术,以SymRK为诱饵筛选百脉根AD-cDNA文库,分离到与SymRK相互作用的蛋白SIE3。SIE3属于最近发现的含CTLH/CRA/RING结构域的新的蛋白家族,在植物中普遍存在,但是这类蛋白的功能目前还不是很清楚。我们主要从以下几个方面对SIE3进行了探索性的研究：
1.通过拼接2个EST表达序列标签Lj-G0027263与Lj-G0032470及同源蛋白比对分析确定SIE3的全长编码序列,然后通过RT-PCR的方法扩增得到其全长cDNA。SIE3开放读码框包含1161个核苷酸,编码的蛋白质由387个氨基酸残基组成。蛋白质序列分析显示SIE3含有三个典型的结构域：CTLH结构域、RanBPM-CRA结构域和RING-finger结构域,其中RING finger结构域是一个特化的C3HC4型RING-finger,即属于一种RING-S/T型RING-finger。三维结构分析表明,SIE3主要以反向平行的二聚体形式存在,并且在酵母中可以自身相互作用。酵母双杂交研究结果表明,全长SIE3与SymRK-PK以及SymRK-EC之间都存在相互作用,并且SIE3蛋白中的RING finger结构域是SIE3与SymRK相互作用所必须的。通过双分子荧光互补(BIFC)以及免疫共沉淀技术证实了SIE3与SymRK的相互作用且主要存在于细胞膜上。
2.泛素连接酶活性研究表明,当泛素活化酶E1和泛素结合酶E2及泛素存在条件下,体外检测到SIE3结合多聚泛素化链后的一系列高分子量蛋白带,说明SIE3具有很强的泛素连接酶活性。通过农杆菌侵染在烟草叶片中共表达SIE3与SymRK,在烟草细胞内检测SIE3连接酶活性。当SIE3存在时,发现SymRK被泛素化修饰的高分子量蛋白带明显增多,由此证实SIE3在体内具有介导SymRK泛素化修饰的功能。同时,体内及半体外泛素化降解分析表明,SIE3不能介导SymRK蛋白泛素化降解,说明SIE3介导SymRK泛素化修饰后行使的是非蛋白泛素化降解功能,具体的机制需要进一步深入研究。
3. SIP1(SymRK interacting protein1)是一个ARID类转录因子,能特异的结合NIN的启动子。其蛋白极不稳定,在烟草叶片中表达的蛋白主要是通过泛素化途径降解。酵母双杂交研究结果表明SIE3能与SIP1相互作用,而且SIE3-N端及SIE3-C端都参与了两者之间的相互作用。进一步通过BIFC的方法证实了两者在植物中的相互作用并发生在细胞膜与细胞核上。烟草体内以及半体外泛素化降解实验表明SIE3能促进SIP1的泛素化降解,并且SIE3同源二聚体在促进SIP1的泛素化降解中不断增加。由此表明SIE3同源二聚体可能是促进SIP1泛素化降解所必须的,且SIP1可能是SIE3除SymRK外的另一个泛素化底物。
4. Real-time RT-PCR研究结果表明SIE3基因在百脉根中呈组成型表达,接种的根中表达量最高,成熟的瘤中表达量最低。在结瘤过程中,接种根瘤菌6天后,根中表达量明显上升,并且10天稳定在较高水平的表达,该结果表明在结瘤早期SIE3基因受结瘤因子诱导表达。通过农杆菌侵染洋葱表皮细胞进行亚细胞定位,发现SIE3定位在细胞膜和细胞核上,少量存在于细胞质中。进一步通过毛根转化以及烟草叶片瞬时表达,在百脉根以及烟草叶片中观察到SIE3同样的定位现象。
5.利用超表达和RNAi干扰技术,研究了SIE3泛素连接酶在百脉根中的共生功能。其研究结果表明,当SIE3超表达后,结瘤数明显增多。而沉默SIE3后,根瘤数显著减少,侵染率也大大降低。进一步通过检测SIE3RNAi后转基因植株中结瘤素基因NIN, ENOD40-2与Lb的表达情况,发现NIN与ENOD40-2基因的表达被抑制了,而对Lb表达没有受影响,表明SIE3主要是在结瘤的早期阶段发挥功能。
The root nodule symbiosis (RNS) between legume plants and rhizobia is the most efficient and productive source of nitrogen fixation, and has critical importance in agriculture and mesology. Nodule symbiosis formation is a tightly regulated process that coordinates the activation of developmental mechanisms to synchronize bacterial infection and organ development and is accompanied by a series of signal transduction. Nod factor signaling is an essential element in the establishment of the symbiosis. During the past decade, a lot of genes have been identified from various symbiotic mutants of the two model legumes:Lotus japonicus and Medicago truncatula. A signaling pathway necessary for Nod factor signal transduction was revealed by genetic dissection of nodulation. The symbiosis receptor kinase, SymRK, is indispensable for rhizobial signaling cascade in legumes and may function at the decision rhizobial enter the plants whether or not. However, little is known about how SymRK receive and transduce the NF signal to downstream components. In this study, using SymRK-EC as a bait to screen a Lotus japonicus AD-cDNA library, we identified a SymRK-interacting E3ligase (SIE3). SIE3represents a novel protein family of containing the CTLH, RanBPM-CRA and RING domains, which are conserved in higher plants with no known biological function till now. The exploratory study of SIE3was mainly focus on the following several aspects in this study.
1. According to the two EST clones Lj-G0027263and Lj-G0032470, and the peptide sequence homology alignment analysis of SIE3, the reconstituted full-length coding region of SIE3was identified. Then we designed primers according to the reconstituted full-length coding region and amplified its cDNA using RNA isolated from L. japonicus roots inoculated with M. loti. The1,161-bp coding region encodes387amino acids. The peptide sequence analysis showed that SIE3containing a CTLH (C-terminal to LisH) motif, a RanBPM-CRA domain and a RING (Really Interesting New Gene) finger domain. The RING finger in SIE3is a degenerated type of C3HC4RING finger, and it belongs to the RING-S/T variant. SIE3exists as a reverse parallel homodimer and the dimerization of SIE3could be detected when expressed in yeast cells. Deletion analysis demonstrated that both SymRK-EC and SymRK-PK can interact with SIE3in yeast, and the RING domain is nessary for the interaction between SIE3and SymRK. BIFC and Co-IP assays showed that SIE3can interact with SymRK in plant and the interaction happens in the plasma membrane.
2. The study of the ubquitin ligase activity of SIE3showed that in the presence of wheat (Triticum aestivum) E1activating enzyme, human E2(UBCh5b) conjugating enzyme and Arabidopsis ubiquitin. SIE3was converted to a mixture of high-molecular weight ubiquitinated protein products, suggesting that SIE3has great ubquitin ligase activity. The assay of detecting the SIE3ligase activity in tobacco cells by co-expression in tobacco leaf cells via agroinfiltration showed that the intensity of the SymRK poly-ubiquitinated products were much stronger in the presence of SIE3. These results suggested that SIE3could mediate the ubiquitination of SymRK in vivo. In vivo and in semi-in-vivo assays demonstrated that SIE3can not promote the ubquitin-dependant degradation of SymRK. It means that there exist a nonproteolytic functions of SIE3-mediated ubiquitination of SymRK, while the detail regulation mechanism need to be further studied.
3. SIP1(SymRK interacting protein1) is a ARID transcription factor, can bind specifically to the nodule inception (NIN) promoter. SIP1protein can be easily degradated, and the degradation of SIP1mainly takes place via the ubiquitination pathway rather than another pathway in N. benthamiana. SIE3can interact with SIP1in yeast, and the deletion analysis showed that both SIE3-N and SIE3-C are nessary for the interaction between SIE3and SIP1. Further more, BIFC assay showed that SIE3can interact with SIP1in plant and the interaction happens in the plasma membrane and nuclei. In vivo and in semi-in-vivo assays demonstrated that SIE3can promote the ubquitin-dependant degradation of SIP1, and the homodimer form of the SIE3-GFP protein was increased with SIP1degradation in SIP1protein semi-in-vivo degradation assay. So SIE3homodimer may be nessary for promoting SIP1degradation and SIP1may be another ubquitination substrate of SIE3except SymRK.
4. Real-time RT-PCR results showed that the SIE3mRNA was present in all tested tissues of L. japonicus plants, Rhizobium-inoculated roots with developing nodules were found to have the highest expression level of SIE3mRNA. The lowest expression was found in mature nodules. During the nodulation period, the expression of SIE3was elevated6days after rhizobial infection and stay at high levels10days post inoculation. These observations demonstrated that the expression of SIE3is induced by Nod factor in the early state of nodulation. SIE3-GFP was expressed in transgenic onion (Allium cepa) epidermal cells by agroinfiltration, and its subcellular localization was found in both the nuclei and plasma membrane, less in cytoplasm. The same subcellular localization could be found in transgenic hairy roots of L. japonicas and transgenic N. benthamiana leaves by hairy root transformation and transient expression in tobacco leaves.
5. Overexpression and RNA interference technologies were used to study the symbiotic function of SIE3ubquitin ligase in Lotus japonicas. And the results showed that Overexpression of SIE3promoted nodulationin transgenic hairy roots. Whereas down-regulation of SIE3transcripts by RNA interference (RNAi) inhibited infection thread development and nodule organogenesis. Through further investigate the expression level of NIN, ENOD40-2and Lb mRNAs in SIE3-RNAi transgenic hairy roots, we found that the expression levels of these genes except Lb were reduced drastically as compared with those in the control hairy roots. These results demonstrate a role of SIE3in the early events of nodulation.
引文
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