植物学报 ›› 2016, Vol. 51 ›› Issue (1): 130-143.DOI: 10.11983/CBB14216
• 专题论坛 • 上一篇
收稿日期:
2014-12-25
接受日期:
2015-03-30
出版日期:
2016-01-01
发布日期:
2016-02-01
通讯作者:
刘建中
作者简介:
? 共同第一作者
基金资助:
Zhen Liu, Xia Liu, Jianzhong Liu*
Received:
2014-12-25
Accepted:
2015-03-30
Online:
2016-01-01
Published:
2016-02-01
Contact:
Liu Jianzhong
About author:
? These authors contributed equally to this paper
摘要: 亚硝基化是近年来新发现的不依赖于环磷酸鸟苷的一氧化氮信号转导途径, 是一氧化氮分子通过共价结合修饰靶蛋白的半胱氨酸残基从而改变其功能的过程。该文重点综述了近年来亚硝基化在细胞死亡和抗病反应这两个紧密关联的生物学过程中的最新研究成果, 总结了亚硝基化通过修饰和调控靶蛋白从而促进或抑制细胞死亡和抗病反应, 并对现有研究结果中某些不一致之处提出自己的观点。最后根据动物学领域的最新研究进展对植物学领域未来亚硝基化的研究方向进行了展望。
刘振, 刘霞, 刘建中. 亚硝基化在植物细胞死亡及防御反应中的作用. 植物学报, 2016, 51(1): 130-143.
Zhen Liu, Xia Liu, Jianzhong Liu. The Roles of Protein S-nitrosylation in Plant Cell Death and Disease Resistance. Chinese Bulletin of Botany, 2016, 51(1): 130-143.
图1 植物胞内蛋白亚硝基化水平的稳态平衡调控 植物体内亚硝基化水平由NO的产生及去亚硝基化的能力决定。植物体内NO可由众多途径产生, 包括NOA1途径、NR途径、质膜NR/NiNOR途径、线粒体途径、多胺途径、过氧化酶体XOR途径和质外体途径。另外, 微生物产生的NO对植物也有一定的影响(Crawford and Guo, 2005; Yu et al., 2014)。生物和非生物胁迫可诱导NO在植物体内的合成。在胁迫条件下, 细胞内NO浓度升高, NO与GSH结合形成GSNO。GSNO是亚硝基化的NO供体, 亚硝基化的实现是由GSNO而并非由NO直接介导。GSNO可将NO反式转移至靶蛋白从而改变蛋白的功能(Liu et al., 2001; Feechan et al., 2005)。GSNOR1和硫氧还蛋白(thioredoxins, TRX)是去亚硝基化的2个关键酶。GSNOR1通过还原和降低植物体内的GSNO水平间接降低蛋白亚硝基化。而TRX-h3和TRX-h5可直接催化蛋白的去亚硝基化(Tada et al., 2008)。
Figure 1 The homeostasis of cellular S-nitrosylation level in plantsThe level of S-nitrosylation in plant cells is determined by balance between the production of NO and the capacity of de-nitrosylation. There are multiple routes for NO production in plants such as NOA1-dependent pathway, NR pathway, plasma-membrane NR/NiNOR pathway, mitochondrial pathway, polyamines pathway, peroxisome (XOR) pathway and apoplast pathway. In addition, micro-organisms also contribute to the NO accumulation in plants (Crawford and Guo, 2005; Yu et al., 2014). Both biotic and abiotic stresses can induce the production of NO. Under stress conditions, NO level is increased in plant cells and as a results, the GSNO is formed in the presence of GSH; GSNO is a major donor of S-nitrosylation and S-nitrosylation is mediated by GSNO rather than by NO directly; NO moiety is transferred from GSNO to proteins in trans and thus the protein functions are altered by this modification (Liu et al., 2001; Feechan et al., 2005). GSNOR1 and thioredoxins (TRX) are two key enzymes involved in de-nitrosylation. Whereas GSNOR1 achieves the protein de-nitrosylation indirectly through reducing cellular level of GSNO, TRX (TRX-h3 and TRX-h5) catalyzes de-nitrosylation directly (Tada et al., 2008).
图2 亚硝基化调控植物细胞死亡 (A) NO通过亚硝基化抑制H2O2分解及还原相关酶造成细胞内过量积累H2O2, 从而促进细胞死亡。cAPX是亚硝基化的靶蛋白, 被亚硝基化后其活性受到抑制。另一方面亚硝基化可导致cAPX的泛素化, 加速其通过蛋白酶体的降解, 从而使细胞内H2O2含量增加, 最终导致细胞死亡(de Pinto et al., 2013)。(B) NO通过亚硝基化质膜上NADPH氧化酶复合体中AtRBOHD亚基的Cys890负反馈抑制其合成H2O2的能力, 从而降低细胞中H2O2的含量及抑制细胞过度死亡(Yun et al., 2011)。(C) NO通过亚硝基化过氧化物氧还酶PrxII E中的Cys121抑制其还原H2O2及过亚硝酸盐(ONOO-)解毒能力。过亚硝酸盐通过不可逆地硝基化(nitration)络氨酸残基而改变蛋白的功能, PrxII E具保护蛋白不被硝基化的功能(Romero-Puertas et al., 2007)。(D) GSNOR1蛋白作为正调控因子参与除草剂百草枯诱导的细胞死亡。除草剂百草枯处理可导致野生型拟南芥死亡, 但不能导致体内积累过量RNS的GSNOR1功能缺失突变体par2-1死亡。ROS具增加细胞内GSNOR1蛋白含量的效应, 而RNS则具降低GSNOR1蛋白含量的效应。GSNOR1作用于ROS的下游参与除草剂百草枯诱导的细胞死亡(Chen et al., 2009)。
Figure 2 Regulation of cell death by S-nitrosylation in plants(A) NO promotes cell death through increasing the accumulation of H2O2 excessively by inhibiting H2O2 detoxifying enzymes. cAPX is a target of S-nitrosylation and its enzyme activity is severely inhibited by S-nitrosylation. In addition, S-nitrosylation of cAPX results in its ubiquitination and degradation by proteasome and thus leads to the cell death by over-accumulation of H2O2 (de Pinto et al., 2013). (B) NO can feedback inhibit H2O2 production through S-nitrosylation of Cys890 of AtRBOHD, a subunit of NADPH oxidase on the plasmamembrane, and as a result, excessive accumulation of H2O2 is relieved and cell death is alleviated (Yun et al., 2011). (C) NO inhibits H2O2 reduction and ONOO- detoxification of PrxII E through S-nitrosylation at Cys121. ONOO- can irreversibly alter protein functions through nitration. PrxII E is an enzyme that can prevent proteins from nitration (Romero-Puertas et al., 2007). (D) GSNOR1 functions as a positive regulator that participates in the cell death induced by paraquat. Application of herbicide paraquat can kill the wild type Arabidopsis Col-0 but not par2-1, a missense mutant of GSNOR1. ROS has an effect in increasing the level of GSNOR1, whereas RSN has the opposite effect. GSNOR1 participates paraquat-induced cell death downstream of ROS (Chen et al., 2009).
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